Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III.

During perceptually guided decisions, correlates of choice are found as upstream as in the primary sensory areas. However, how well these choice signals align with early sensory representations, a prerequisite for their interpretation as feedforward substrates of perception, remains an open question. We designed a two alternative forced choice task (2AFC) in which male mice compared stimulation frequencies applied to two adjacent vibrissae. The optogenetic silencing of individual columns in the primary somatosensory cortex (wS1) resulted in predicted shifts of psychometric functions, demonstrating that perception depends on focal, early sensory representations. Functional imaging of layer II/III single neurons revealed mixed coding of stimuli, choices and engagement in the task. Neurons with multi-whisker suppression display improved sensory discrimination and had their activity increased during engagement in the task, enhancing selectively representation of the signals relevant to solving the task. From trial to trial, representation of stimuli and choice varied substantially, but mostly orthogonally to each other, suggesting that perceptual variability does not originate from wS1 fluctuations but rather from downstream areas. Together, our results highlight the role of primary sensory areas in forming a reliable sensory substrate that could be used for flexible downstream decision processes.

Heuristics in risky decision-making relate to preferential representation of information.

When making choices, individuals differ from one another, as well as from normativity, in how they weigh different types of information. One explanation for this relates to idiosyncratic preferences in what information individuals represent when evaluating choice options. Here, we test this explanation with a simple risky-decision making task, combined with magnetoencephalography (MEG). We examine the relationship between individual differences in behavioral markers of information weighting and neural representation of stimuli pertinent to incorporating that information. We find that the extent to which individuals (N = 19) behaviorally weight probability versus reward information is related to how preferentially they neurally represent stimuli most informative for making probability and reward comparisons. These results are further validated in an additional behavioral experiment (N = 88) that measures stimulus representation as the latency of perceptual detection following priming. Overall, the results suggest that differences in the information individuals consider during choice relate to their risk-taking tendencies.

The active time model of concurrent choice.

The following paper describes a steady-state model of concurrent choice, termed the active time model (ATM). ATM is derived from maximization principles and is characterized by a semi-Markov process. The model proposes that the controlling stimulus in concurrent variable-interval (VI) VI schedules of reinforcement is the time interval since the most recent response, termed here "the active interresponse time" or simply "active time." In the model after a response is generated, it is categorized by a function that relates active times to switch/stay probabilities. In the paper the output of ATM is compared with predictions made by three other models of operant conditioning: melioration, a version of scalar expectancy theory (SET), and momentary maximization. Data sets considered include preferences in multiple-concurrent VI VI schedules, molecular choice patterns, correlations between switching and perseveration, and molar choice proportions. It is shown that ATM can account for all of these data sets, while the other models produce more limited fits. However, rather than argue that ATM is the singular model for concurrent VI VI choice, a consideration of its concept space leads to the conclusion that operant choice is multiply-determined, and that an adaptive viewpoint-one that considers experimental procedures both as selecting mechanisms for animal choice as well as tests of the controlling variables of that choice-is warranted.

Learning to Choose: Behavioral Dynamics Underlying the Initial Acquisition of Decision-Making.

Current theories of decision-making propose that decisions arise through competition between choice options. Computational models of the decision process estimate how quickly information about choice options is integrated and how much information is needed to trigger a choice. Experiments using this approach typically report data from well-trained participants. As such, we do not know how the decision process evolves as a decision-making task is learned for the first time. To address this gap, we used a behavioral design separating learning the value of choice options from learning to make choices. We trained male rats to respond to single visual stimuli with different reward values. Then, we trained them to make choices between pairs of stimuli. Initially, the rats responded more slowly when presented with choices. However, as they gained experience in making choices, this slowing reduced. Response slowing on choice trials persisted throughout the testing period. We found that it was specifically associated with increased exponential variability when the rats chose the higher value stimulus. Additionally, our analysis using drift diffusion modeling revealed that the rats required less information to make choices over time. These reductions in the decision threshold occurred after just a single session of choice learning. These findings provide new insights into the learning process of decision-making tasks. They suggest that the value of choice options and the ability to make choices are learned separately and that experience plays a crucial role in improving decision-making performance.

Loss, gain and choice difficulty in gambling patients: Neural and behavioural processes.

Impaired decision-making is often displayed by individuals suffering from gambling disorder (GD). Since there are a variety of different phenomena influencing decision-making, we focused in this study on the effects of GD on neural and behavioural processes related to loss aversion and choice difficulty. Behavioural responses as well as brain images of 23 patients with GD and 20 controls were recorded while they completed a mixed gambles task, where they had to decide to either accept or reject gambles with different amounts of potential gain and loss. We found no behavioural loss aversion in either group and no group differences regarding loss and gain-related choice behaviour, but there was a weaker relation between choice difficulty and decision time in patients with GD. Similarly, we observed no group differences in processing of losses or gains, but choice difficulty was weaker associated with brain activity in the right anterior insula and anterior cingulate cortex in patients with GD. Our results showed for the first time the effects of GD on neural processes related to choice difficulty. In addition, our findings on choice difficulty give new insights on the psychopathology of GD and on neural processes related to impaired decision-making in GD.

Foraging in a non-foraging task: Fitness maximization explains human risk preference dynamics under changing environment.

Changes in risk preference have been reported when making a series of independent risky choices or non-foraging economic decisions. Behavioral economics has put forward various explanations for specific changes in risk preference in non-foraging tasks, but a consensus regarding the general principle underlying these effects has not been reached. In contrast, recent studies have investigated human economic risky choices using tasks adapted from foraging theory, which require consideration of past choices and future opportunities to make optimal decisions. In these foraging tasks, human economic risky choices are explained by the ethological principle of fitness maximization, which naturally leads to dynamic risk preference. Here, we conducted two online experiments to investigate whether the principle of fitness maximization can explain risk preference dynamics in a non-foraging task. Participants were asked to make a series of independent risky economic decisions while the environmental richness changed. We found that participants' risk preferences were influenced by the current and past environments, making them more risk-averse during and after the rich environment compared to the poor environment. These changes in risk preference align with fitness maximization. Our findings suggest that the ethological principle of fitness maximization might serve as a generalizable principle for explaining dynamic preferences, including risk preference, in human economic decision-making.

Graded decisions in the human brain.

Decision-makers objectively commit to a definitive choice, yet at the subjective level, human decisions appear to be associated with a degree of uncertainty. Whether decisions are definitive (i.e., concluding in all-or-none choices), or whether the underlying representations are graded, remains unclear. To answer this question, we recorded intracranial neural signals directly from the brain while human subjects made perceptual decisions. The recordings revealed that broadband gamma activity reflecting each individual's decision-making process, ramped up gradually while being graded by the accumulated decision evidence. Crucially, this grading effect persisted throughout the decision process without ever reaching a definite bound at the time of choice. This effect was most prominent in the parietal cortex, a brain region traditionally implicated in decision-making. These results provide neural evidence for a graded decision process in humans and an analog framework for flexible choice behavior.

Localized and global representation of prior value, sensory evidence, and choice in male mouse cerebral cortex.

Adaptive behavior requires integrating prior knowledge of action outcomes and sensory evidence for making decisions while maintaining prior knowledge for future actions. As outcome- and sensory-based decisions are often tested separately, it is unclear how these processes are integrated in the brain. In a tone frequency discrimination task with two sound durations and asymmetric reward blocks, we found that neurons in the medial prefrontal cortex of male mice represented the additive combination of prior reward expectations and choices. The sensory inputs and choices were selectively decoded from the auditory cortex irrespective of reward priors and the secondary motor cortex, respectively, suggesting localized computations of task variables are required within single trials. In contrast, all the recorded regions represented prior values that needed to be maintained across trials. We propose localized and global computations of task variables in different time scales in the cerebral cortex.

No immediate attentional bias towards or choice bias for male secondary sexual characteristics in Bornean orang-utans (Pongo pygmaeus).

Primate faces provide information about a range of variant and invariant traits, including some that are relevant for mate choice. For example, faces of males may convey information about their health or genetic quality through symmetry or facial masculinity. Because perceiving and processing such information may have bearing on the reproductive success of an individual, cognitive systems are expected to be sensitive to facial cues of mate quality. However, few studies have investigated this topic in non-human primate species. Orang-utans are an interesting species to test mate-relevant cognitive biases, because they are characterised by male bimaturism: some adult males are fully developed and bear conspicuous flanges on the side of their face, while other males look relatively similar to females. Here, we describe two non-invasive computerised experiments with Bornean orang-utans (Pongo pygmaeus), testing (i) immediate attention towards large flanges and symmetrical faces using a dot-probe task (N = 3 individuals; 2F) and (ii) choice bias for pictures of flanged males over unflanged males using a preference test (N = 6 individuals; 4F). In contrast with our expectations, we found no immediate attentional bias towards either large flanges or symmetrical faces. In addition, individuals did not show a choice bias for stimuli of flanged males. We did find exploratory evidence for a colour bias and energy efficiency trade-offs in the preference task. We discuss our null results and exploratory results in the context of the evolutionary history of Bornean orang-utans, and provide suggestions for a more biocentric approach to the study of orang-utan cognition.

Differential representation of sensory information and behavioral choice across layers of the mouse auditory cortex.

The activity of neurons in sensory areas sometimes covaries with upcoming choices in decision-making tasks. However, the prevalence, causal origin, and functional role of choice-related activity remain controversial. Understanding the circuit-logic of decision signals in sensory areas will require understanding their laminar specificity, but simultaneous recordings of neural activity across the cortical layers in forced-choice discrimination tasks have not yet been performed. Here, we describe neural activity from such recordings in the auditory cortex of mice during a frequency discrimination task with delayed report, which, as we show, requires the auditory cortex. Stimulus-related information was widely distributed across layers but disappeared very quickly after stimulus offset. Choice selectivity emerged toward the end of the delay period-suggesting a top-down origin-but only in the deep layers. Early stimulus-selective and late choice-selective deep neural ensembles were correlated, suggesting that the choice-selective signal fed back to the auditory cortex is not just action specific but develops as a consequence of the sensory-motor contingency imposed by the task.

Volatile working memory representations crystallize with practice.

Working memory, the process through which information is transiently maintained and manipulated over a brief period, is essential for most cognitive functions1-4. However, the mechanisms underlying the generation and evolution of working-memory neuronal representations at the population level over long timescales remain unclear. Here, to identify these mechanisms, we trained head-fixed mice to perform an olfactory delayed-association task in which the mice made decisions depending on the sequential identity of two odours separated by a 5 s delay. Optogenetic inhibition of secondary motor neurons during the late-delay and choice epochs strongly impaired the task performance of the mice. Mesoscopic calcium imaging of large neuronal populations of the secondary motor cortex (M2), retrosplenial cortex (RSA) and primary motor cortex (M1) showed that many late-delay-epoch-selective neurons emerged in M2 as the mice learned the task. Working-memory late-delay decoding accuracy substantially improved in the M2, but not in the M1 or RSA, as the mice became experts. During the early expert phase, working-memory representations during the late-delay epoch drifted across days, while the stimulus and choice representations stabilized. In contrast to single-plane layer 2/3 (L2/3) imaging, simultaneous volumetric calcium imaging of up to 73,307 M2 neurons, which included superficial L5 neurons, also revealed stabilization of late-delay working-memory representations with continued practice. Thus, delay- and choice-related activities that are essential for working-memory performance drift during learning and stabilize only after several days of expert performance.

Differences in Discounting Behavior and Brain Responses for Food and Money Reward.

Most neuroeconomic research seeks to understand how value influences decision-making. The influence of reward type is less well understood. We used functional magnetic resonance imaging (fMRI) to investigate delay discounting of primary (i.e., food) and secondary rewards (i.e., money) in 28 healthy, normal-weighted participants (mean age = 26.77; 18 females). To decipher differences in discounting behavior between reward types, we compared how well-different option-based statistical models (exponential, hyperbolic discounting) and attribute-wise heuristic choice models (intertemporal choice heuristic, dual reasoning and implicit framework theory, trade-off model) captured the reward-specific discounting behavior. Contrary to our hypothesis of different strategies for different rewards, we observed comparable discounting behavior for money and food (i.e., exponential discounting). Higher k values for food discounting suggest that individuals decide more impulsive if confronted with food. The fMRI revealed that money discounting was associated with enhanced activity in the right dorsolateral prefrontal cortex, involved in executive control; the right dorsal striatum, associated with reward processing; and the left hippocampus, involved in memory encoding/retrieval. Food discounting, instead, was associated with higher activity in the left temporoparietal junction suggesting social reinforcement of food decisions. Although our findings do not confirm our hypothesis of different discounting strategies for different reward types, they are in line with the notion that reward types have a significant influence on impulsivity with primary rewards leading to more impulsive choices.

Attribute latencies causally shape intertemporal decisions.

Intertemporal choices - decisions that play out over time - pervade our life. Thus, how people make intertemporal choices is a fundamental question. Here, we investigate the role of attribute latency (the time between when people start to process different attributes) in shaping intertemporal preferences using five experiments with choices between smaller-sooner and larger-later rewards. In the first experiment, we identify attribute latencies using mouse-trajectories and find that they predict individual differences in choices, response times, and changes across time constraints. In the other four experiments we test the causal link from attribute latencies to choice, staggering the display of the attributes. This changes attribute latencies and intertemporal preferences. Displaying the amount information first makes people more patient, while displaying time information first does the opposite. These findings highlight the importance of intra-choice dynamics in shaping intertemporal choices and suggest that manipulating attribute latency may be a useful technique for nudging.

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.

Healthy adults favor stable left/right hand choices over performance at an unconstrained reach-to-grasp task.

Reach-to-grasp actions are fundamental to the daily activities of human life, but few methods exist to assess individuals' reaching and grasping actions in unconstrained environments. The Block Building Task (BBT) provides an opportunity to directly observe and quantify these actions, including left/right hand choices. Here we sought to investigate the motor and non-motor causes of left/right hand choices, and optimize the design of the BBT, by manipulating motor and non-motor difficulty in the BBT's unconstrained reach-to-grasp task. We hypothesized that greater motor and non-motor (e.g. cognitive/perceptual) difficulty would drive increased usage of the dominant hand. To test this hypothesis, we modulated block size (large vs. small) to influence motor difficulty, and model complexity (10 vs. 5 blocks per model) to influence non-motor difficulty, in healthy adults (n = 57). Our data revealed that increased motor and non-motor difficulty led to lower task performance (slower task speed), but participants only increased use of their dominant hand only under the most difficult combination of conditions: in other words, participants allowed their performance to degrade before changing hand choices, even though participants were instructed only to optimize performance. These results demonstrate that hand choices during reach-to grasp actions are more stable than motor performance in healthy right-handed adults, but tasks with multifaceted difficulties can drive individuals to rely more on their dominant hand.

Autoshaped impulsivity: Some explorations with a neural network model.

This study evaluated the effect of delay and magnitude of reinforcement in Pavlovian contingencies, extending the understanding of the phenomenon of autoshaped impulsivity as described in Alcalá's thesis (2017) and Burgos and García-Leal (2015). The effects of adding a trace interval were analyzed on the maintained responses of impulsive choice, seen as the preference of a small and immediate reinforcer over a larger and delayed one, and the role of the contextual unit, as well as the inhibitory units according to the Diffuse Discrepancy Model. In the Simulation, the model with inhibitory units was used, trained in two signals with different delays and reinforcement magnitudes, and subsequently presented concurrently in choice tasks without reinforcement nor learning, using an ABA within-subject design. In general, the DD model successfully simulated the phenomenon of autoshaped impulsivity, consistent with studies from Alcalá's thesis (2017), Burgos and García-Leal (2015), and Picker and Poling (1982). It also predicted the elimination of this effect (autoshaped impulsivity) after introducing a trace interval. The observed results and their implications are discussed, as well as possible future studies with animals and humans.

The neural representation of metacognition in preferential decision-making.

Humans regularly assess the quality of their judgements, which helps them adjust their behaviours. Metacognition is the ability to accurately evaluate one's own judgements, and it is assessed by comparing objective task performance with subjective confidence report in perceptual decisions. However, for preferential decisions, assessing metacognition in preference-based decisions is difficult because it depends on subjective goals rather than the objective criterion. Here, we develop a new index that integrates choice, reaction time, and confidence report to quantify trial-by-trial metacognitive sensitivity in preference judgements. We found that the dorsomedial prefrontal cortex (dmPFC) and the right anterior insular were more activated when participants made bad metacognitive evaluations. Our study suggests a crucial role of the dmPFC-insula network in representing online metacognitive sensitivity in preferential decisions.

Win-win or lose-lose: Children prefer the form of equality.

In middle childhood, children's sense of fairness further develops, they are willing to pay a cost to maintain equality. Win-win and lose-lose are two forms of equality. Win-win equality refers to both parties maximizing benefits, while lose-lose equality means both parties incurring the maximum loss. Win-win equality allows third party upholding fairness to gain more reputational benefits without the violator being punished, embodying the principle of "benefiting oneself without harming others". On the other hand, lose-lose equality is a more deterrent form of fairness with the violator getting punished, and the third-party might experience a situation of "effort without appreciation." However, the specific form of equality which school-aged children prefer still requires further exploration. Therefore, adopting the dictator game paradigm of third-party punishment, we design two experiments to investigate the fairness preference of first to fourth-grade children when acting as a third party and to clarify patterns of age-related changes. Study 1 (N = 111) explored children's preferred form of fairness under advantageous inequity conditions. Study 2 (N = 122) further examined children's fairness preferences in disadvantageous inequity situations. The findings suggest that when confronted with inequitable distributions, whether rooted in disadvantageous or advantageous inequity, children display a notable tendency to utilize third-party punishment to achieve an equal allocation. Meanwhile, this tendency strengthens as they progress in grade levels. Notably, children consistently manifest a preference for win-win equality, highlighting their inclination towards mutually beneficial outcomes.

Performance errors during rodent learning reflect a dynamic choice strategy.

Humans, even as infants, use cognitive strategies, such as exploration and hypothesis testing, to learn about causal interactions in the environment. In animal learning studies, however, it is challenging to disentangle higher-order behavioral strategies from errors arising from imperfect task knowledge or inherent biases. Here, we trained head-fixed mice on a wheel-based auditory two-choice task and exploited the intra- and inter-animal variability to understand the drivers of errors during learning. During learning, performance errors are dominated by a choice bias, which, despite appearing maladaptive, reflects a dynamic strategy. Early in learning, mice develop an internal model of the task contingencies such that violating their expectation of reward on correct trials (by using short blocks of non-rewarded "probe" trials) leads to an abrupt shift in strategy. During the probe block, mice behave more accurately with less bias, thereby using their learned stimulus-action knowledge to test whether the outcome contingencies have changed. Despite having this knowledge, mice continued to exhibit a strong choice bias during reinforced trials. This choice bias operates on a timescale of tens to hundreds of trials with a dynamic structure, shifting between left, right, and unbiased epochs. Biased epochs also coincided with faster motor kinematics. Although bias decreased across learning, expert mice continued to exhibit short bouts of biased choices interspersed with longer bouts of unbiased choices and higher performance. These findings collectively suggest that during learning, rodents actively probe their environment in a structured manner to refine their decision-making and maintain long-term flexibility.

Risk-Taking Is Associated with Decreased Subjective Value Signals and Increased Prediction Error Signals in the Hot Columbia Card Task.

It remains a pressing concern to understand how neural computations relate to risky decisions. However, most observations of brain-behavior relationships in the risk-taking domain lack a rigorous computational basis or fail to emulate of the dynamic, sequential nature of real-life risky decision-making. Recent advances emphasize the role of neural prediction error (PE) signals. We modeled, according to prospect theory, the choices of n = 43 human participants (33 females, 10 males) performing an EEG version of the hot Columbia Card Task, featuring rounds of sequential decisions between stopping (safe option) and continuing with increasing odds of a high loss (risky option). Single-trial regression EEG analyses yielded a subjective value signal at centroparietal (300-700 ms) and frontocentral (>800 ms) electrodes and in the delta band, as well as PE signals tied to the feedback-related negativity, P3a, and P3b, and in the theta band. Higher risk preference (total number of risky choices) was linked to attenuated subjective value signals but increased PE signals. Higher P3-like activity associated with the most positive PE in each round predicted stopping in the present round but not risk-taking in the subsequent round. Our findings indicate that decreased representation of decision values and increased sensitivity to winning despite low odds (positive PE) facilitate risky choices at the subject level. Strong neural responses when gains are least expected (the most positive PE on each round) adaptively contribute to safer choices at the trial-by-trial level but do not affect risky choice at the round-by-round level.