Neural dynamics of two players when using nonverbal cues to gauge intentions to cooperate during the Prisoner's Dilemma Game.

Social interaction is a fundamental part of our daily lives; however, exactly how our brains use social cues to determine whether to cooperate without being exploited remains unclear. In this study, we used an electroencephalography (EEG) hyperscanning approach to investigate the effect of face-to-face contact on the brain mechanisms underlying the decision to cooperate or defect in an iterated version of the Prisoner's Dilemma Game. Participants played the game either in face-to-face or face-blocked conditions. The face-to-face interaction led players to cooperate more often, providing behavioral evidence for the use of these nonverbal cues in their social decision-making. In addition, the EEG hyperscanning identified temporal dynamics and inter-brain synchronization across the cortex, providing evidence for involvement of these regions in the processing of face-to-face cues to read each other's intent to cooperate. Most notably, the power of the alpha frequency band (8-13Hz) in the right temporoparietal region immediately after seeing a round outcome significantly differed between face-to-face and face-blocked conditions and predicted whether an individual would adopt a 'cooperation' or 'defection' strategy. Moreover, inter-brain synchronies within this time and frequency range reflected the use of these strategies. This study provides evidence for how the cortex uses nonverbal social cues to determine other's intentions, and highlights the significance of power in the alpha band and inter-brain phase synchronizations in high-level socio-cognitive processing.

Vulnerability-Based Critical Neurons, Synapses, and Pathways in the Caenorhabditis elegans Connectome.

Determining the fundamental architectural design of complex nervous systems will lead to significant medical and technological advances. Yet it remains unclear how nervous systems evolved highly efficient networks with near optimal sharing of pathways that yet produce multiple distinct behaviors to reach the organism's goals. To determine this, the nematode roundworm Caenorhabditis elegans is an attractive model system. Progress has been made in delineating the behavioral circuits of the C. elegans, however, many details are unclear, including the specific functions of every neuron and synapse, as well as the extent the behavioral circuits are separate and parallel versus integrative and serial. Network analysis provides a normative approach to help specify the network design. We investigated the vulnerability of the Caenorhabditis elegans connectome by performing computational experiments that (a) "attacked" 279 individual neurons and 2,990 weighted synaptic connections (composed of 6,393 chemical synapses and 890 electrical junctions) and (b) quantified the effects of each removal on global network properties that influence information processing. The analysis identified 12 critical neurons and 29 critical synapses for establishing fundamental network properties. These critical constituents were found to be control elements-i.e., those with the most influence over multiple underlying pathways. Additionally, the critical synapses formed into circuit-level pathways. These emergent pathways provide evidence for (a) the importance of backward locomotion, avoidance behavior, and social feeding behavior to the organism; (b) the potential roles of specific neurons whose functions have been unclear; and

Bursts and heavy tails in temporal and sequential dynamics of foraging decisions.

A fundamental understanding of behavior requires predicting when and what an individual will choose. However, the actual temporal and sequential dynamics of successive choices made among multiple alternatives remain unclear. In the current study, we tested the hypothesis that there is a general bursting property in both the timing and sequential patterns of foraging decisions. We conducted a foraging experiment in which rats chose among four different foods over a continuous two-week time period. Regarding when choices were made, we found bursts of rapidly occurring actions, separated by time-varying inactive periods, partially based on a circadian rhythm. Regarding what was chosen, we found sequential dynamics in affective choices characterized by two key features: (a) a highly biased choice distribution; and (b) preferential attachment, in which the animals were more likely to choose what they had previously chosen. To capture the temporal dynamics, we propose a dual-state model consisting of active and inactive states. We also introduce a satiation-attainment process for bursty activity, and a non-homogeneous Poisson process for longer inactivity between bursts. For the sequential dynamics, we propose a dual-control model consisting of goal-directed and habit systems, based on outcome valuation and choice history, respectively. This study provides insights into how the bursty nature of behavior emerges from the interaction of different underlying systems, leading to heavy tails in the distribution of behavior over time and choices.

Relevance of animal models of subarachnoid hemorrhage for examining neurobehavioral changes.

BACKGROUND AND PURPOSE: For many years survival and neurological functionality of patients were the main outcome measures after treatment of intracranial aneurysms. But, the variable outcomes of patients operated on in a delayed fashion or before the aneurysm rupture indicate that more precise measures are needed for assessment of not only the neurological but also the neuropsychological outcome. However, development and testing of such new tools requires better understanding of pathomechanisms of neurobehavioral changes evoked by aneurysmal subarachnoid hemorrhage (aSAH), which can be achieved using animal models. METHODS: We reviewed and selected (1) animal models developed to investigate delayed cerebral vasospasm that could be useful for examining effects of brain injury evoked by aSAH and (2) a battery of neurobehavioral animal testing that can be used for assessment of patients after aSAH. RESULTS: For every species used as an aSAH model, a battery of neurobehavioral test exists. CONCLUSION: Albeit some limitations must be recognized, research using animal models of SAH should continue to play a critical role in assessment of cognitive and behavioral functions after aSAH.

How 'who someone is' and 'what they did' influences gossiping about them.

To understand, predict, and help correct each other's actions we need to maintain accurate, up-to-date knowledge of people, and communication is a critical means by which we gather and disseminate this information. Yet the conditions under which we communication social information remain unclear. Testing hypotheses generated from our theoretical framework, we examined when and why social information is disseminated about an absent third party: i.e., gossiped. Gossip scenarios presented to participants (e.g., "Person-X cheated on their exam") were based on three key factors: (1) target (ingroup, outgroup, or celebrity), (2) valence (positive or negative), and (3) content. We then asked them (a) whether they would spread the information, and (b) to rate it according to subjective valence, ordinariness, interest level, and emotion. For ratings, the scenarios participants chose to gossip were considered to have higher valence (whether positive or negative), to be rarer, more interesting, and more emotionally evocative; thus showing that the paradigm was meaningful to subjects. Indeed, for target, valence, and content, a repeated-measures ANOVA found significant effects for each factor independently, as well as their interactions. The results supported our hypotheses: e.g., for target, more gossiping about celebrities and ingroup members (over strangers); for valence, more about negative events overall, and yet for ingroup members, more positive gossiping; for content, more about moral topics, with yet all domains of social content communicated depending on the situation-context matters, influencing needs. The findings suggest that social knowledge sharing (i.e., gossip) involves sophisticated calculations that require our highest sociocognitive abilities, and provide specific hypotheses for future examination of neural mechanisms.

Multitasking of attention and memory functions in the primate prefrontal cortex.

In motor and sensory areas of cortex, neuronal activity often depends on the location of a movement target or a sensory stimulus, with each neuron tuned to a single part of space called a preferred direction (when motor) or a receptive field (when sensory). As we previously reported, some neurons in the monkey prefrontal cortex are tuned to two parts of space, which we interpreted as reflecting attention and working memory, respectively. Monkeys performed a behavioral task in which they attended to a visual stimulus at one location while remembering a second place, and these locations were varied from trial to trial to assess spatial tuning. Most spatially tuned neurons specialized in either attentional or mnemonic processing, but about one-third of the cells showed tuning for both. Here, we show that the latter population, called multitasking neurons, improves the encoding of both the attended and remembered locations. These neurons do so for three reasons: (1) the preferred directions for attention and for working memory usually differ (and often diametrically oppose one another), (2) they have stronger tuning than specialized cells, and (3) pairs of multitasking neurons represent these cognitive parameters more efficiently than pairs that include even a single specialized cell. These findings suggest that multitasking neurons provide a computational advantage for behaviors that place simultaneous demands on two or more cognitive processes.

Retrospective Evaluation of Sequential Events and the Influence of Preference-Dependent Working Memory: A Computational Examination.

Humans organize sequences of events into a single overall experience, and evaluate the aggregated experience as a whole, such as a generally pleasant dinner, movie, or trip. However, such evaluations are potentially computationally taxing, and so our brains must employ heuristics (i.e., approximations). For example, the peak-end rule hypothesis suggests that we average the peaks and end of a sequential event vs. integrating every moment. However, there is no general model to test viable hypotheses quantitatively. Here, we propose a general model and test among multiple specific ones, while also examining the role of working memory. The models were tested with a novel picture-rating task. We first compared averaging across entire sequences vs. the peak-end heuristic. Correlation tests indicated that averaging prevailed, with peak and end both still having significant prediction power. Given this, we developed generalized order-dependent and relative-preference-dependent models to subsume averaging, peak and end. The combined model improved the prediction power. However, based on limitations of relative-preference-including imposing a potentially arbitrary ranking among preferences-we introduced an absolute-preference-dependent model, which successfully explained the remembered utilities. Yet, because using all experiences in a sequence requires too much memory as real-world settings scale, we then tested "windowed" models, i.e., evaluation within a specified window. The windowed (absolute) preference-dependent (WP) model explained the empirical data with long sequences better than without windowing. However, because fixed-windowed models harbor their own limitations-including an inability to capture peak-event influences beyond a fixed window-we then developed discounting models. With (absolute) preference-dependence added to the discounting rate, the results showed that the discounting model reflected the actual working memory of the participants, and that the preference-dependent discounting (PD) model described different features from the WP model. Taken together, we propose a combined WP-PD model as a means by which people evaluate experiences, suggesting preference-dependent working-memory as a significant factor underlying our evaluations.

A Computational Model of Attention Control in Multi-Attribute, Context-Dependent Decision Making.

Real-life decisions often require a comparison of multi-attribute options with various benefits and costs, and the evaluation of each option depends partly on the others in the choice set (i.e., the choice context). Although reinforcement learning models have successfully described choice behavior, how to account for multi-attribute information when making a context-dependent decision remains unclear. Here we develop a computational model of attention control that includes context effects on multi-attribute decisions, linking a context-dependent choice model with a reinforcement learning model. The overall model suggests that the distinctiveness of attributes guides an individual's preferences among multi-attribute options via an attention-control mechanism that determines whether choices are selectively biased toward the most distinctive attribute (selective attention) or proportionally distributed based on the relative distinctiveness of attributes (divided attention). To test the model, we conducted a behavioral experiment in rhesus monkeys, in which they made simple multi-attribute decisions over three conditions that manipulated the degree of distinctiveness between alternatives: (1) four foods of different size and calorie; (2) four pieces of the same food in different colors; and (3) four identical pieces of food. The model simulation of the choice behavior captured the preference bias (i.e., overall preference structure) and the choice persistence (repeated choices) in the empirical data, providing evidence for the respective influences of attention and memory on preference bias and choice persistence. Our study provides insights into computations underlying multi-attribute decisions, linking attentional control to decision-making processes.

Preference-based serial decisions are counterintuitively influenced by emotion regulation and conscientiousness.

Our decisions have a temporally distributed order, and different choice orders (e.g., choosing preferred items first or last) can lead to vastly different experiences. We previously found two dominant strategies (favorite-first and favorite-last) in a preference-based serial choice setting (the 'sushi problem'). However, it remains unclear why these two opposite behavioral patterns arise: i.e., the mechanisms underlying them. Here we developed a novel serial-choice task, using pictures based on attractiveness, to test for a possible shared mechanism with delay discounting, the 'peak-end' bias (i.e., preference for experienced sequences that end well), or working-memory capacity. We also collected psychological and clinical metric data on personality, depression, anxiety, and emotion regulation. We again found the two dominant selection strategies. However, the results of the delay, peak-end bias, and memory capacity tasks were not related to serial choice, while two key psychological metrics were: emotion regulation and conscientiousness (with agreeableness also marginally related). Favorite-first strategists actually regulated emotions better, suggesting better tolerance of negative outcomes. Whereas participants with more varied strategies across trials were more conscientious (and perhaps agreeable), suggesting that they were less willing to settle for a single, simpler strategy. Our findings clarify mechanisms underlying serial choice and show that it may reflect a unique ability to organize choices into sequences of events.

Neural Correlates of Public Apology Effectiveness.

Apologizing is an effective interpersonal conflict resolution strategy, but whether, and if so how, organizations should issue public apologies after crises remains less clear. To assuage the fear of possible crisis reoccurrence, public apologies may be effective when they provide a comprehensive account of what happened and clarify actions taken by the company to address the problems. If this is so, public apologies may be most effective when the crisis source resides within the organization itself, suggesting that the company has control over it. In the current study, we first tested this hypothesis by presenting participants with multiple crisis scenarios (e.g., ignition failures in a new car model) followed by one of two written apologies: one stating that the crisis source was internal to and controllable by the organization, and the other external and uncontrollable. The internal-controllable (IC) public apology proved most effective. We then examined the neural basis of this public apology assessment and found that the frontal polar cortex appears to mediate the assessment of organizational control, and the angular gyrus uses the information for the apology assessment. Examination of complex social interactions, such as the public's reaction to corporate crises, helps to elucidate high-level brain function.

Abstraction promotes creative problem-solving in rhesus monkeys.

Abstraction allows us to discern regularities beyond the specific instances we encounter. It also promotes creative problem-solving by enabling us to consider unconventional problem solutions. However, the mechanisms by which this occurs are not well understood. Because it is often difficult to isolate human high-level cognitive processes, we utilized a nonhuman primate model, in which rhesus monkeys appear to use similar processes to consider an unconventional solution to the difficult reverse-reward problem: i.e., given the choice between a better and worse food option they must select the worse one to receive the better one. After solving this problem with only one specific example-one vs. four half-peanuts-three of four monkeys immediately transferred to novel cases: novel quantities, food items, non-food items, and to the choice between a larger, but inferior vegetable and a smaller, but superior food item (either grape or marshmallow), in which they selected the inferior vegetable to receive the superior option. Thus, we show that nonhuman animals have the capacity to comprehend abstract non-perceptual features, to infer them from one specific case, and to use them to override the natural preference to select the superior option. Critically, we also found that three monkeys had a large learning and performance advantage over the fourth monkey who showed less generalization from the original one and four half-peanuts. This difference suggests that abstraction promoted problem-solving via cascading activation from the two food item options to the relation between them, thus providing access to an initially nonapparent problem solution.

Representation of attended versus remembered locations in prefrontal cortex.

A great deal of research on the prefrontal cortex (PF), especially in nonhuman primates, has focused on the theory that it functions predominantly in the maintenance of short-term memories, and neurophysiologists have often interpreted PF's delay-period activity in the context of this theory. Neuroimaging results, however, suggest that PF's function extends beyond the maintenance of memories to include aspects of attention, such as the monitoring and selection of information. To explore alternative interpretations of PF's delay-period activity, we investigated the discharge rates of single PF neurons as monkeys attended to a stimulus marking one location while remembering a different, unmarked location. Both locations served as potential targets of a saccadic eye movement. Although the task made intensive demands on short-term memory, the largest proportion of PF neurons represented attended locations, not remembered ones. The present findings show that short-term memory functions cannot account for all, or even most, delay-period activity in the part of PF explored. Instead, PF's delay-period activity probably contributes more to the process of attentional selection.

Nucleus accumbens shell moderates preference bias during voluntary choice behavior.

The nucleus accumbens (NAc) shell lies anatomically at a critical intersection within the brain's reward system circuitry, however, its role in voluntary choice behavior remains unclear. Rats with electrolytic lesions in the NAc shell were tested in a novel foraging paradigm. Over a continuous two-week period they freely chose among four nutritionally identical but differently flavored food pellets by pressing corresponding levers. We examined the lesion's effects on three behavioral dynamics components: motivation (when to eat), preference bias (what to choose) and persistence (how long to repeat the same choice). The lesion led to a marked increase in the preference bias: i.e., increased selection of the most-preferred choice option, and decreased selection of the others. We found no effects on any other behavioral measures, suggesting no effect on motivation or choice persistence. The results implicate the NAc shell in moderating the instrumental valuation process by inhibiting excessive bias toward preferred choice options.

Heightened aversion to risk and loss in depressed patients with a suicide attempt history.

Suicide attempters have been found to be impaired in decision-making; however, their specific biases in evaluating uncertain outcomes remain unclear. Here we tested the hypothesis that suicidal behavior is associated with heightened aversion to risk and loss, which might produce negative predictions about uncertain future events. Forty-five depressed patients with a suicide attempt history, 47 nonsuicidal depressed patients, and 75 healthy controls participated in monetary decision-making tasks assessing risk and loss aversion. Suicide attempters compared with the other groups exhibited greater aversion to both risk and loss during gambles involving potential loss. Risk and loss aversion correlated with each other in the depressed patients, suggesting that a common pathophysiological mechanism underlies these biases. In addition, emotion regulation via suppression, a detrimental emotional control strategy, was positively correlated with loss aversion in the depressed patients, also implicating impairment in regulatory processes. A preliminary fMRI study also found disrupted neural responses to potential gains and losses in the subgenual anterior cingulate cortex, insula cortex, and left amygdala, brain regions involved in valuation, emotion reactivity, and emotion regulation. The findings thus implicate heightened negative valuation in decision-making under risk, and impaired emotion regulation in depressed patients with a history of suicide attempts.

Competitive control of cognition in rhesus monkeys.

The brain has evolved different approaches to solve problems, but the mechanisms that determine which approach to take remain unclear. One possibility is that control progresses from simpler processes, such as associative learning, to more complex ones, such as relational reasoning, when the simpler ones prove inadequate. Alternatively, control could be based on competition between the processes. To test between these possibilities, we posed the support problem to rhesus monkeys using a tool-use paradigm, in which subjects could pull an object (the tool) toward themselves to obtain an otherwise out-of-reach goal item. We initially provided one problem exemplar as a choice: for the correct option, a food item placed on the support tool; for the incorrect option, the food item placed off the tool. Perceptual cues were also correlated with outcome: e.g., red, triangular tool correct, blue, rectangular tool incorrect. Although the monkeys simply needed to touch the tool to register a response, they immediately pulled it, reflecting a relational reasoning process between themselves and another object (Rself-other), rather than an associative one between the arbitrary touch response and reward (Aresp-reward). Probe testing then showed that all four monkeys used a conjunction of perceptual features to select the correct option, reflecting an associative process between stimuli and reward (Astim-reward). We then added a second problem exemplar and subsequent testing revealed that the monkeys switched to using the on/off relationship, reflecting a relational reasoning process between two objects (Rother-other). Because behavior appeared to reflect Rself-other rather than Aresp-reward, and Astim-reward prior to Rother-other, our results suggest that cognitive processes are selected via competitive control dynamics.

Inhibitory control and response selection in problem solving: how cotton-top tamarins (Saguinus oedipus) overcome a bias for selecting the larger quantity of food.

When presented with a choice between 1 and 3 pieces of food in a type of reversed contingency task, 4 cotton-top tamarins (Saguinus oedipus) consistently chose the 3 pieces of food and received nothing, even though the choice of 1 piece would have yielded 3. However, in a task in which the tamarins received the 1 piece of food when they chose it, all subjects learned to select 1 over 3. Thus, the tamarins' prior failure on the reversed contingency task did not result entirely from an inherent inability to suppress the prepotent response of reaching to the larger of 2 quantities of food. After the experience of selecting the smaller quantity and receiving it, all of the tamarins solved the version of the reversed contingency task that they failed initially. These results suggest that the tamarins' initial failure may have reflected a difficulty with selecting an alternative response option.

The relationship between problem solving and inhibitory control: cotton-top tamarin (Saguinus oedipus) performance on a reversed contingency task.

To explore the relationship between problem solving and inhibitory control, the authors present 4 experiments on cotton-top tamarins (Saguinus oedipus) using a reverse-reward contingency task. In Experiment 1, 1 group of tamarins was given a choice between a small and a large quantity of food. Whichever quantity the tamarins reached for first, they received the alternative. The tamarins consistently picked the larger quantity, thereby receiving the smaller. A 2nd group of tamarins was given the same task, except that if they reached for the larger quantity of food, they received nothing. The tamarins continued to pick the larger quantity, even though this resulted in no food. In addition, most of the tamarins continued to pick the larger quantity even when the food payoff for choosing the smaller quantity was increased (Experiment 2) or when the visual salience of the food was reduced (Experiment 3). Experiment 4 was based on the finding that chimpanzees (Pan troglodytes) that have been trained on the concept of number can solve the reversed contingency task if the food is replaced by Arabic numerals. With the help of a color association, and a higher cost incurred by picking the color associated with 3 food items, the tamarins learned to pick the color associated with 1 food item. These results are compared with those obtained from studies of other primate species, highlighting the importance of comparative studies of problem solving that use comparable methods.

Risky business: rhesus monkeys exhibit persistent preferences for risky options.

Rhesus monkeys have been shown to prefer risky over safe options in experiential decision-making tasks. These findings might be due, however, to specific contextual factors, such as small amounts of fluid reward and minimal costs for risk-taking. To better understand the factors affecting decision-making under risk in rhesus monkeys, we tested multiple factors designed to increase the stakes including larger reward amounts, distinct food items rather than fluid reward, a smaller number of trials per session, and risky options with greater variation that also included non-rewarded outcomes. We found a consistent preference for risky options, except when the expected value of the safe option was greater than the risky option. Thus, with equivalent mean utilities between the safe and risky options, rhesus monkeys appear to have a robust preference for the risky options in a broad range of circumstances, akin to the preferences found in human children and some adults in similar tasks. One account for this result is that monkeys make their choices based on the salience of the largest payoff, without integrating likelihood and value across trials. A related idea is that they fail to override an impulsive tendency to select the option with the potential to obtain the highest possible outcome. Our results rule out strict versions of both accounts and contribute to an understanding of the diversity of risky decision-making among primates.

Rats exhibit reference-dependent choice behavior.

Human preferences depend on whether a chosen outcome appears to be a loss or a gain compared with what had been expected, i.e., in comparison to a reference point. Because reference dependence has such a strong influence on human decision-making, it is important to uncover its origins, which will in turn help delineate the underlying mechanisms. It remains unknown whether rats use reference points in decision-making, and yet, the study of rats could help address the question of whether reference dependence is evolutionarily conserved among mammals and could provide a nonhuman animal model to investigate the neural mechanisms underlying this important cognitive process. The aim of the current study was to determine whether rats show reference-dependent choice behavior. We developed a novel paradigm by modifying the "T" maze by installing "pockets" to the left and right of the "T" stem that held reward pellets so rats would potentially develop reference values for each option prior to choice. We found that the rats were indeed sensitive to the way alternatives were presented. That is, they exhibited reference-dependent choice behavior by avoiding the choice option framed as a loss (e.g., having four reward pellets in the pocket, but receiving only one), at least under conditions with certain outcomes and clear differences between the reference and outcome quantities. Despite the small number of rats in this study, this species-level capacity suggests that reference dependence in general and loss aversion in particular may be conserved traits that evolved at or before the emergence of mammals.