Autistic adults show enhanced generosity to socially distant others.

LAY ABSTRACT: Autistic people show differences in their social behaviour. But how autism affects decisions to share resources, an important part of cooperation, was previously unclear. In our study, participants made decisions about how to share money with different people, including people they felt close to, such as a friend, and people they felt less close to, such as a stranger. We found that compared to a group of non-autistic participants, autistic adults shared more money overall and this was driven by greater generosity to strangers. The results suggest that autistic adults were more generous because they made fair decisions (an equal split of the money) more consistently regardless of how close they felt to the person they were sharing with. By showing that autistic adults display greater generosity, our results could help to change public perceptions of autism and potentially improve opportunities for autistic people.

50-kHz ultrasonic vocalizations do not signal social anhedonia in transgenic DISC1 rats.

Patients diagnosed with neuropsychiatric disorders, such as autism and schizophrenia, suffer from disorganized speech. The disrupted-in-schizophrenia 1 (DISC1) protein pathway is considered a risk factor for the development of several psychiatric disorders and plays an important role in the dysregulation of dopamine (DA), which in turn plays an important role in the regulation of ultrasonic vocalizations (USVs) in rats. Moreover, the DISC1 protein pathway has been identified as a cause of social anhedonia, that is, a decrease in the drive for social interactions. USVs transmit specific affective information to other rats, with 50-kHz calls indicating a positive affective state in rats. Dysregulation of the dopaminergic system impacts the qualitative and quantitative features of USVs, such as duration, peak frequency, and the call rate. In this study, we thus used a well-established transgenic DISC1 (tgDISC1) rat line to investigate whether the neural (decreased DA levels in the dorsal striatum, amygdala, and hippocampus (HPC)) and behavioral (social anhedonia) features of tgDISC1 rats could be manifested through the modulation of their 50-kHz USVs. Analyses of three features (call rate, duration, and peak frequency) of all 50-kHz revealed no significant differences between groups, suggesting decreased DA levels in the dorsal striatum and amygdala, and HPC may affect social interaction but leave 50-kHz USV production intact.

Discounting of Future Rewards and Punishments in Rats.

Temporal reward discounting describes the decrease of value of a reward as a function of delay. Decision-making between future aversive outcomes is much less studied, and there is no clear decision pattern across studies; while some authors suggest that human and nonhuman animals prefer sooner over later painful shocks, others found the exact opposite. In a series of three experiments, Long-Evans rats chose between differently timed electric shocks and rewards in a T-maze. In experiment 1, rats chose between early and late painful shocks with identical, long reward delays; in experiment 2, they chose between early reward and early shocks, or late rewards and late shocks; in experiment 3, they chose between early and late rewards, with identical, short delays to the shock. We tested the predictions of two competing hypotheses: the aversive discounting theory assumes that future shocks are discounted, and, hence, less unpleasant than early shocks. The utility from anticipation theory implies that rats derive negative utility from waiting for the shock; late shocks should, hence, be more unpleasant than early shocks. We did not find unanimous evidence for either theory. Instead, our results are more consistent with the post hoc idea that shocks may have negative spill-over effects on reward values, the closer in time a shock is to a subsequent reward, the stronger the reward is devalued. Interestingly and consistent with our theory, we find that, depending on the temporal shock-reward contiguity, rats can be brought to prefer later over sooner rewards of identical magnitudes.

Lesions of nucleus accumbens shell abolish socially transmitted food preferences.

Rats adapt their food choices to conform to their conspecifics' dietary preferences. The nucleus accumbens shell is a relevant brain region to process reward-related and motivated behaviours and social information. Here, we hypothesize that the integrity of the nucleus accumbens shell is necessary to show socially transmitted food preferences. We made excitotoxic and sham lesions of nucleus accumbens shell in male Long-Evans rats who performed a social transmission of food preference task. In this task, observer rats revealed their original preference for one out of two food options. Afterward, they were exposed to a demonstrator rat who was fed with the observer's originally non-preferred food, and the observer's food choices were sampled again. Sham lesioned observer rats changed their food preferences following interaction with the demonstrator, specifically by increasing the intake of their originally non-preferred food type. This interaction-related change in preference was not found after nucleus accumbens shell lesions. The lesion effects on choice were not the consequence of impaired social or non-social motivation, anxiety or sensory or motor function, suggesting that they reflected a genuine deficit in social reward revaluation. These results highlight the role of nucleus accumbens shell in revaluating food rewards to match a conspecific's preferences.

On the reliability of individual economic rationality measurements.

A contemporary research agenda in behavioral economics and neuroeconomics aims to identify individual differences and (neuro)psychological correlates of rationality. This research has been widely received in important interdisciplinary and field outlets. However, the psychometric reliability of such measurements of rationality has been presumed without enough methodological scrutiny. Drawing from multiple original and published datasets (in total over 1,600 participants), we unequivocally show that contemporary measurements of rationality have moderate to poor reliability according to common standards. Further analyses of the variance components, as well as a allowing participants to revise previous choices, suggest that this is driven by low between-subject variance rather than high measurement error. As has been argued previously for other behavioral measurements, this poses a challenge to the predominant correlational research designs and the search for sociodemographic or neural predictors. While our results draw a sobering picture of the prospects of contemporary measurements of rationality, they are not necessarily surprising from a theoretical perspective, which we outline in our discussion.

Social anhedonia as a Disrupted-in-Schizophrenia 1-dependent phenotype.

Deficits in social interaction or social cognition are key phenotypes in a variety of chronic mental diseases, yet, their modeling and molecular dissection are only in their infancy. The Disrupted-in-Schizophrenia 1 (DISC1) signaling pathway is considered to play a role in different psychiatric disorders such as schizophrenia, depression, and biopolar disorders. DISC1 is involved in regulating the dopaminergic neurotransmission in, among others, the mesolimbic reward system. A transgenic rat line tgDISC1 has been introduced as a model system to study behavioral phenotypes associated with abnormal DISC1 signaling pathways. Here, we evaluated the impact of impaired DISC1 signaling on social (social interaction) and non-social (sucrose) reward preferences in the tgDISC1 animal model. In a plus-maze setting, rats chose between the opportunity for social interaction with an unfamiliar juvenile conspecific (social reward) or drinking sweet solutions with variable sucrose concentrations (non-social reward). tgDISC1 rats differed from wild-type rats in their social, but not in their non-social reward preferences. Specifically, DISC1 rats showed a lower interest in interaction with the juvenile conspecific, but did not differ from wild-type rats in their preference for higher sucrose concentrations. These results suggest that disruptions of the DISC1 signaling pathway that is associated with altered dopamine transmission in the brain result in selective deficits in social motivation reminiscent of phenotypes seen in neuropsychiatric illness.

Variations in progesterone and estradiol across the menstrual cycle predict generosity toward socially close others.

The human tendency to share goods with others at personal costs declines across the perceived social distance to them, an observation termed social discounting. Cumulating evidence suggests that social preferences are influenced by the agent's neurohormonal state. Here we tested whether endogenous fluctuations in steroid hormone compositions across the menstrual cycle were associated with differences in generosity in a social discounting task. Adult healthy, normally-cycling, women made incentivized decisions between high selfish rewards for themselves and lower generous rewards for themselves but also for other individuals at variable social distances from their social environment. We determined participants' current levels of menstrual-cycle-dependent steroid hormones via salivary sampling. Results revealed that the increase in progesterone levels as well as the decrease in estradiol levels, but not changes in testosterone or cortisol, across the menstrual cycle, accounted for increased generosity specifically toward socially close others, but not toward remote strangers.

Influence of memory processes on choice-consistency.

Choice-consistency is considered a hallmark of rational value-based choice. However, because the cognitive apparatus supporting decision-making is imperfect, real decision-makers often show some degree of choice inconsistency. Cognitive models are necessary to complement idealized choice axioms with attention, perception and memory processes. Specifically, compelling theoretical work suggests that the (imperfect) retention of choice-relevant memories might be important for choice-consistency, but this hypothesis has not been tested directly. We used a novel multi-attribute visual choice paradigm to experimentally test the influence of memory retrieval of exemplars on choice-consistency. Our manipulation check confirmed that our retention interval manipulation successfully reduced memory representation strength. Given this, we found strong evidence against our hypothesis that choice-consistency decreases with increasing retention time. However, quality controls indicated that the choice-consistency of our participants was non-discernable from random behaviour. In addition, an exploratory analysis showed essentially no test-retest reliability of choice-consistency between two observations. Taken together, this suggests the presence of a floor effect in our data and, thus, low data quality for conclusively evaluating our hypotheses. Further exploration tentatively suggested a high difficulty of discriminating between the choice objects driving this floor effect.

Distinct Profiles of 50 kHz Vocalizations Differentiate Between Social Versus Non-social Reward Approach and Consumption.

Social animals tend to possess an elaborate vocal communication repertoire, and rats are no exception. Rats utilize ultrasonic vocalizations (USVs) to communicate information about a wide range of socially relevant cues, as well as information regarding the valence of the behavior and/or surrounding environment. Both quantitative and qualitative acoustic properties of these USVs are thought to communicate context-specific information to conspecifics. Rat USVs have been broadly categorized into 22 and 50 kHz call categories, which can be further classified into subtypes based on their sonographic features. Recent research indicates that the 50 kHz calls and their various subtype profiles may be related to the processing of social and non-social rewards. However, only a handful of studies have investigated USV elicitation in the context of both social and non-social rewards. Here, we employ a novel behavioral paradigm, the social-sucrose preference test, that allowed us to measure rats' vocal responses to both non-social (i.e., 2, 5, and 10% sucrose) and social reward (interact with a Juvenile rat), presented concurrently. We analyzed adult male Long-Evans rats' vocal responses toward social and non-social rewards, with a specific focus on 50 kHz calls and their 14 subtypes. We demonstrate that rats' preference and their vocal responses toward a social reward were both influenced by the concentration of the non-social reward in the maze. In other words, rats showed a trade-off between time spent with non-social or social stimuli along with increasing concentrations of sucrose, and also, we found a clear difference in the emission of flat and frequency-modulated calls in the social and non-social reward zones. Furthermore, we report that the proportion of individual subtypes of 50 kHz calls, as well as the total USV counts, showed variation across different types of rewards as well. Our findings provide a thorough overview of rat vocal responses toward non-social and social rewards and are a clear depiction of the variability in the rat vocalization repertoire, establishing the role of call subtypes as key players driving context-specific vocal responses of rats.

Trier social stress test and food-choice: Behavioral, self-report & hormonal data.

A sample of 144 participants underwent the Trier Social Stress Test (TSST), a psychosocial stress manipulation involving a mock interview and a mental arithmetic task, or a matched control procedure. Physiological stress was estimated via a collection of 7 saliva samples over the course of the experiment analysed for cortisol and alpha-amylase, as well as via the mean heart-rate measured before and during the experimental manipulation. Subjective stress was assessed via the Positive and Negative Affect Scale as well as four Visual Analogue Scales at 6 points over the time course of the experiment. Participants solved an incentive-compatible food-choice task before, immediately after and in the aftermath of the experimental manipulation. In each trial of the food-choice task, participants had to choose one out of a set of two to seven snack bundles. Each snack bundle consisted of specific amounts of a sweet or salty snack and a fruit or vegetable. The snacks for both categories were selected to be similarly attractive according to the previously provided online ratings of the participants. The design of the food-choice task allows for the calculation of revealed preference consistency indices. The dataset further contains several self-report questionnaires administered to the participants before the experimental session, including the Trier Inventory of Chronic Stress.

Arbitration between insula and temporoparietal junction subserves framing-induced boosts in generosity during social discounting.

Generosity toward others declines across the perceived social distance to them. Here, participants chose between selfish and costly generous options in two conditions: in the gain frame, a generous choice yielded a gain to the other; in the loss frame, it entailed preventing the loss of a previous endowment to the other. Social discounting was reduced in the loss compared to the gain frame, implying increased generosity toward strangers. Using neuroimaging tools, we found that while activity in the temporoparietal junction (TPJ) and the ventromedial prefrontal cortex (VMPFC) was associated with generosity in the gain frame, the insular cortex was selectively recruited during generous choices in the loss frame. We provide support for a network-model according to which TPJ and insula differentially subserve generosity by modulating value signals in the VMPFC in a frame-dependent fashion. These results extend our understanding of the insula role in nudging prosocial behavior in humans.

The effects of acute and chronic stress on choice consistency.

Important decisions are often made under some degree of stress. It is now well-established that acute stress affects preferences and priorities in our decisions. However, it is hard to make a general case on the net impact of stress on decision-making quality in a normative sense as evidence for or against a direct effect of stress on decision-making quality is sparse. Here, we used the revealed preference framework of choice consistency to investigate decision-making quality without the assumption of an objectively correct choice. Specifically, we tested whether acute stress influences choice consistency in a time dependent fashion. A sample of 144 participants solved a food choice task before, immediately after and in the aftermath of the Trier Social Stress Test (TSST) or a matched control procedure. We confirmed the effectiveness of our stress manipulation via an array of subjective and physiological stress measures. Using Bayesian statistics, we found strong evidence against an effect of acute stress on choice consistency. However, we found exploratory evidence for a negative association of self-reported chronic stress and choice consistency. We discuss our results in the context of previous findings of stress effects on choice consistency and preference changes.

Anterior Cingulate Cortex Lesions Abolish Budget Effects on Effort-Based Decision-Making in Rat Consumers.

Demand theory can be applied to analyze how animal consumers change their selection of commodities in response to changes in commodity prices, given budget constraints. Previous work has shown that demand elasticities in rats differed between uncompensated budget conditions in which the budget available to be spent on the commodities (e.g., the finite number of discrete operants to "purchase" rewards in two-alternative fixed-ratio schedules) was kept constant, and compensated budget conditions in which the budget was adjusted so that consumers could potentially continue to obtain the original reward bundles. Here, we hypothesized that rat anterior cingulate cortex (ACC) was necessary to produce this budget effect on demand elasticities. We applied excitotoxic or sham lesions to ACC in rats performing an effort task in which the prices of liquid vanilla or chocolate rewards (the effort required to obtain rewards) and the budget (the total number of operants) was manipulated. When reward prices changed, and the budget was compensated, all rats adjusted their demand for chocolate and vanilla accordingly. In sham-lesioned rats, changes in demand were even more pronounced when the budget was not compensated for the price changes. By contrast, ACC-lesioned animals did not show this additional budget effect. An in-depth comparison of the rats' choice patterns showed that, unlike sham rats, ACC-lesioned animals failed to maximize session-bundle utility after price/budget changes, revealing deficits in higher-order choice-strategy adaptations. Our results suggest a novel role of ACC in considering purchasing power during complex cost-benefit value computations.SIGNIFICANCE STATEMENT Anterior cingulate cortex (ACC) is important for allocating effort in cost-benefit calculations in animals and humans. Economic theory prescribes that the value of the costs in cost-benefit analyses not only depends on the net nominal costs required to purchase a reward, but also on the available budget resources, i.e., on the budget's "purchasing value." We asked whether ACC, a region implicated in effort-based decision-making and reward comparisons, is required for computing the value of effort relative to a budget constraint. Applying demand theory to describe rat choices in a rodent effort allocation task with varying effort prices and budgets, we show that ACC integrity was necessary for computing purchasing power, a core variable in economic choice theory.

A decision-neuroscientific intervention to improve cognitive recovery after stroke.

Functional recovery after stroke is dose-dependent on the amount of rehabilitative training. However, rehabilitative training is subject to motivational hurdles. Decision neuroscience formalizes drivers and dampers of behaviour and provides strategies for tipping motivational trade-offs and behaviour change. Here, we used one such strategy, upfront voluntary choice restriction ('precommitment'), and tested if it can increase the amount of self-directed rehabilitative training in severely impaired stroke patients. In this randomized controlled study, stroke patients with working memory deficits (n = 83) were prescribed daily self-directed gamified cognitive training as an add-on to standard therapy during post-acute inpatient neurorehabilitation. Patients allocated to the precommitment intervention could choose to restrict competing options to self-directed training, specifically the possibility to meet visitors. This upfront choice restriction was opted for by all patients in the intervention group and highly effective. Patients in the precommitment group performed the prescribed self-directed gamified cognitive training twice as often as control group patients who were not offered precommitment [on 50% versus 21% of days, Pcorr = 0.004, d = 0.87, 95% confidence interval (CI95%) = 0.31 to 1.42], and, as a consequence, reached a 3-fold higher total training dose (90.21 versus 33.60 min, Pcorr = 0.004, d = 0.83, CI95% = 0.27 to 1.38). Moreover, add-on self-directed cognitive training was associated with stronger improvements in visuospatial and verbal working memory performance (Pcorr = 0.002, d = 0.72 and Pcorr = 0.036, d = 0.62). Our neuroscientific decision add-on intervention strongly increased the amount of effective cognitive training performed by severely impaired stroke patients. These results warrant a full clinical trial to link decision-based neuroscientific interventions directly with clinical outcome.

Vicarious reward unblocks associative learning about novel cues in male rats.

Many species, including rats, are sensitive to social signals and their valuation is important in social learning. Here we introduce a task that investigates if mutual reward delivery in male rats can drive associative learning. We found that when actor rats have fully learned a stimulus-self-reward association, adding a cue that predicted additional reward to a partner unblocked associative learning about this cue. By contrast, additional cues that did not predict partner reward remained blocked from acquiring positive associative value. Importantly, this social unblocking effect was still present when controlling for secondary reinforcement but absent when social information exchange was impeded, when mutual reward outcomes were disadvantageously unequal to the actor or when the added cue predicted reward delivery to an empty chamber. Taken together, these results suggest that mutual rewards can drive associative learning in rats and is dependent on vicariously experienced social and food-related cues.

5-HT1A receptor agonism in the basolateral amygdala increases mutual-reward choices in rats.

Rats show mutual-reward preferences, i.e., they prefer options that result in a reward for both themselves and a conspecific partner to options that result in a reward for themselves, but not for the partner. In a previous study, we have shown that lesions of the basolateral amygdala (BLA) reduced choices for mutual rewards. Here, we aimed to explore the role of 5-HT1A receptors within the BLA in mutual-reward choices. Rats received daily injections of either 50 or 25 ng of the 5-HT1A receptor agonist 8-OH-DPAT or a vehicle solution into the BLA and mutual-reward choices were measured in a rodent prosocial choice task. Compared to vehicle injections, 8-OH-DPAT significantly increased mutual-reward choices when a conspecific was present. By contrast, mutual-reward choices were significantly reduced by 8-OH-DPAT injections in the presence of a toy rat. The effect of 8-OH-DPAT injections was statistically significant during the expression, but not during learning of mutual-reward behavior, although an influence of 8-OH-DPAT injections on learning could not be excluded. There were no differences between 8-OH-DPAT-treated and vehicle-treated rats in general reward learning, behavioral flexibility, locomotion or anxiety. In this study, we have shown that repeated injections of the 5-HT1A receptor agonist 8-OH-DPAT have the potential to increase mutual-reward choices in a social setting without affecting other behavioral parameters.

Social Neuroscience: How the Brain Attends to the Joys and Pains of Others.

Social interaction entails keeping an eye on good and bad things happening to others. A new study suggests that neurons in rat anterior cingulate cortex encode the attention paid to rewards and shocks to conspecifics, independently of empathically feeling their joy and pain.

Age differences in predicting working memory performance from network-based functional connectivity.

Deterioration in working memory capacity (WMC) has been associated with normal aging, but it remains unknown how age affects the relationship between WMC and connectivity within functional brain networks. We therefore examined the predictability of WMC from fMRI-based resting-state functional connectivity (RSFC) within eight meta-analytically defined functional brain networks and the connectome in young and old adults using relevance vector machine in a robust cross-validation scheme. Particular brain networks have been associated with mental functions linked to WMC to a varying degree and are associated with age-related differences in performance. Comparing prediction performance between the young and old sample revealed age-specific effects: In young adults, we found a general unpredictability of WMC from RSFC in networks subserving WM, cognitive action control, vigilant attention, theory-of-mind cognition, and semantic memory, whereas in older adults each network significantly predicted WMC. Moreover, both WM-related and WM-unrelated networks were differently predictive in older adults with low versus high WMC. These results indicate that the within-network functional coupling during task-free states is specifically related to individual task performance in advanced age, suggesting neural-level reorganization. In particular, our findings support the notion of a decreased segregation of functional brain networks, deterioration of network integrity within different networks and/or compensation by reorganization as factors driving associations between individual WMC and within-network RSFC in older adults. Thus, using multivariate pattern regression provided novel insights into age-related brain reorganization by linking cognitive capacity to brain network integrity.

CBPtools: a Python package for regional connectivity-based parcellation.

Regional connectivity-based parcellation (rCBP) is a widely used procedure for investigating the structural and functional differentiation within a region of interest (ROI) based on its long-range connectivity. No standardized software or guidelines currently exist for applying rCBP, making the method only accessible to those who develop their own tools. As such, there exists a discrepancy between the laboratories applying the procedure each with their own software solutions, making it difficult to compare and interpret the results. Here, we outline an rCBP procedure accompanied by an open source software package called CBPtools. CBPtools is a Python (version 3.5+) package that allows users to run an extensively evaluated rCBP analysis workflow on a given ROI. It currently supports two modalities: resting-state functional connectivity and structural connectivity based on diffusion-weighted imaging, along with support for custom connectivity matrices. Analysis parameters are customizable and the workflow can be scaled to a large number of subjects using a parallel processing environment. Parcellation results with corresponding validity metrics are provided as textual and graphical output. Thus, CBPtools provides a simple plug-and-play, yet customizable way to conduct rCBP analyses. By providing an open-source software we hope to promote reproducible and comparable rCBP analyses and, importantly, make the rCBP procedure readily available. Here, we demonstrate the utility of CBPtools using a voluminous data set on an average compute-cluster infrastructure by performing rCBP on three ROIs prominently featured in parcellation literature.

10,000 social brains: Sex differentiation in human brain anatomy.

In human and nonhuman primates, sex differences typically explain much interindividual variability. Male and female behaviors may have played unique roles in the likely coevolution of increasing brain volume and more complex social dynamics. To explore possible divergence in social brain morphology between men and women living in different social environments, we applied probabilistic generative modeling to ~10,000 UK Biobank participants. We observed strong volume effects especially in the limbic system but also in regions of the sensory, intermediate, and higher association networks. Sex-specific brain volume effects in the limbic system were linked to the frequency and intensity of social contact, such as indexed by loneliness, household size, and social support. Across the processing hierarchy of neural networks, different conditions for social interplay may resonate in and be influenced by brain anatomy in sex-dependent ways.