Papers by Marijn van Wingerden
Neuron, 2012
Neural activity in orbitofrontal cortex has been linked to flexible representations of stimulus-o... more Neural activity in orbitofrontal cortex has been linked to flexible representations of stimulus-outcome associations. Such value representations are known to emerge with learning, but the neural mechanisms supporting this phenomenon are not well understood. Here, we provide evidence for a causal role for NMDA receptors (NMDARs) in mediating spike pattern discriminability, neural plasticity, and rhythmic synchronization in relation to evaluative stimulus processing and decision making. Using tetrodes, single-unit spike trains and local field potentials were recorded during local, unilateral perfusion of an NMDAR blocker in rat OFC. In the absence of behavioral effects, NMDAR blockade severely hampered outcome-selective spike pattern formation to olfactory cues, relative to control perfusions. Moreover, NMDAR blockade shifted local rhythmic synchronization to higher frequencies and degraded its linkage to stimulus-outcome selective coding. These results demonstrate the importance of NMDARs for cue-outcome associative coding in OFC during learning and illustrate how NMDAR blockade disrupts network dynamics.
Callous-unemotional traits – the insensitivity to other's welfare and well-being – are characteri... more Callous-unemotional traits – the insensitivity to other's welfare and well-being – are characterized by a lack of empathy. They are characteristic of psychopathy and can be found in other antisocial disorders, such as conduct disorder. Because of the increasing prevalence of antisocial disorders and the rising societal costs of violence and aggression, it is of great importance to elucidate the psychological and physiological mechanisms underlying callousness in the search for pharmacological treatments. One promising avenue is to create a relevant animal model to explore the neural bases of callousness. Here, we review recent advances in rodent models of pro-social choice that could be applied to probe the absence of pro-sociality as a proxy of callous behavior, and provide future directions for the exploration of the neural substrates of callousness.
Disadvantageous inequity aversion (IA) is a behavioural response to an inequitable outcome distri... more Disadvantageous inequity aversion (IA) is a behavioural response to an inequitable outcome distribution yielding a smaller reward to oneself than to a conspecific, given comparable efforts to obtain the reward. This behavioural response aims to minimize unfair reward distributions. It has been proposed to be essential for the emergence of cooperation. Humans show choice patterns compatible with IA and, as recently suggested, cooperative nonhuman species such as primates, corvids and dogs also respond negatively to disadvantageous inequitable outcomes. Here, we asked whether rats are sensitive to such inequitable outcomes. In a double T-maze apparatus, actor rats could choose to enter one of two different compartments after which a conspecific (partner rat) entered the adjoining partner compartment. One side of the paired compartments was associated with an equitable reward distribution (identical amount for the actor and the partner) whereas entry into the other paired compartment led to an inequitable reward distribution (in which the partner received a larger reward). Both compartments yielded an identical reward for the actor. Using a within-subjects design, we compared the actor rats' choices in the social condition with a nonsocial baseline control condition in which a toy rat replaced the partner rat. Actor rats exhibited disadvantageous IA: they preferred equitable outcomes in the social, but not the toy condition. Moreover, there was large variability in IA between rats. This heterogeneity in social preference could be partly explained by a social-hierarchy-dependent sensitivity to IA, as dominant animals showed higher IA than subordinate animals. Our study provides evidence for social-hierarchy-dependent disadvantageous IA in social vertebrates. Our findings are consistent with the notion that a sense of fairness may have evolved long before humans emerged. IA may therefore be a basic organizational principle, shared by many social species, that shapes the intricate social dynamics of individuals interrelating in larger groups.
Can You Trust a Rat? Using Animal Models to Investigate the Neural Basis of Trust Like Behavior
Social Cognition, 2015
A Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats
Current Topics in Behavioral Neurosciences, 2016
Although the use of neuroimaging techniques has revealed much about the neural correlates of soci... more Although the use of neuroimaging techniques has revealed much about the neural correlates of social decision making (SDM) in humans, it remains poorly understood how social stimuli are represented, and how social decisions are implemented at the neural level in humans and in other species. To address this issue, the establishment of novel animal paradigms allowing a broad spectrum of neurobiological causal manipulations and neurophysiological recordings provides an exciting tool to investigate the neural implementation of social valuation in the brain. Here, we discuss the potential of a rodent model, Rattus norvegicus, for the understanding of SDM and its neural underpinnings. Particularly, we consider recent data collected in a rodent prosocial choice task within a social reinforcement framework and discuss factors that could drive SDM in rodents.
Inequity aversion in rats, Rattus norvegicus
Animal Behaviour, 2016
In a recent study, we demonstrated that rats prefer mutual rewards in a Prosocial Choice Task. He... more In a recent study, we demonstrated that rats prefer mutual rewards in a Prosocial Choice Task. Here, employing the same task, we show that the integrity of basolateral amygdala was necessary for the expression of mutual reward preferences. Actor rats received bilateral excitotoxic (n = 12) or sham lesions (n = 10) targeting the basolateral amygdala and were subsequently tested in a Prosocial Choice Task where they could decide between rewarding (‘‘Both Reward”) or not rewarding a partner rat (‘‘Own Reward”), either choice yielding identical reward to the actors themselves. To manipulate the social context and control for secondary reinforcement sources, actor rats were paired with either a partner rat (partner condition) or with an inanimate rat toy (toy condition). Sham-operated animals revealed a significant preference for the Both-Reward-option in the partner condition, but not in the toy condition. Amygdala-lesioned animals exhibited significantly lower Both-Reward preferences than the sham group in the partner but not in the toy condition, suggesting that basolateral amygdala was required for the expression of mutual reward preferences. Critically, in a reward magnitude discrimination task in the same experimental setup, both sham-operated and amygdala-lesioned animals preferred large over small rewards, suggesting that amygdala lesion effects were restricted to decision making in social contexts, leaving self-oriented behavior unaffected
Exogenous cortisol causes a shift from deliberative to intuitive thinking
Psychoneuroendocrinology, 2015
People often rely on intuitive judgments at the expense of deliberate reasoning, but what determi... more People often rely on intuitive judgments at the expense of deliberate reasoning, but what determines the dominance of intuition over deliberation is not well understood. Here, we employed a psychopharmacological approach to unravel the role of two major endocrine stress mediators, cortisol and noradrenaline, in cognitive reasoning. Healthy participants received placebo, cortisol (hydrocortisone) and/or yohimbine, a drug that increases noradrenergic stimulation, before performing the cognitive reflection test (CRT). We found that cortisol impaired performance in the CRT by biasing responses toward intuitive, but incorrect answers. Elevated stimulation of the noradrenergic system, however, had no effect. We interpret our results in the context of the dual systems theory of judgment and decision making. We propose that cortisol causes a shift from deliberate, reflective cognition toward automatic, reflexive information processing.
A friend in need: Time-dependent effects of stress on social discounting in men
Hormones and Behavior, 2015
ABSTRACT Stress is often associated with a tend-and-befriend response, a putative coping mechanis... more ABSTRACT Stress is often associated with a tend-and-befriend response, a putative coping mechanism where people behave generously towards others in order to invest in social relationships to seek comfort and mutual protection. However, this increase in generosity is expected to be directed only towards a delimited number of socially close, but not distant individuals, because it would be maladaptive to befriend everyone alike. In addition, the endocrinological stress response follows a distinct temporal pattern, and it is believed that tend-and-befriend tendencies can be observed mainly under acute stress. By contrast, the aftermath (>1 hour after) of stress is associated with endocrinological regulatory processes that are proposed to cause increased executive control and reduced emotional reactivity, possibly eliminating the need to tend-and-befriend. In the present experiment, we set out to investigate how these changes immediately and >1 hour after a stressful experience affect social-distance-dependent generosity levels, a phenomenon called social discounting. We hypothesized that stress has a time-dependent effect on social discounting, with decisions made shortly after (20 min), but not 90 min after stress showing increased generosity particularly to close others. We found that men tested 20 min after stressor onset indeed showed increased generosity towards close but not distant others compared to non-stressed men or men tested 90 minutes after stressor onset. These findings contribute to our understanding on how stress affects prosocial behavior by highlighting the importance of social closeness and the timing of stress relative to the decision as modulating factors in this type of decision making in men. Copyright © 2015. Published by Elsevier Inc.
Budget Constraints Affect Male Rats’ Choices between Differently Priced Commodities
PLOS ONE, 2015
Demand theory can be applied to analyse how a human or animal consumer changes her selection of c... more Demand theory can be applied to analyse how a human or animal consumer changes her selection of commodities within a certain budget in response to changes in price of those commodities. This change in consumption assessed over a range of prices is defined as demand elasticity. Previously, income-compensated and income-uncompensated price changes have been investigated using human and animal consumers, as demand theory predicts different elasticities for both conditions. However, in these studies, demand elasticity was only evaluated over the entirety of choices made from a budget. As compensating budgets changes the number of attainable commodities relative to uncompensated conditions, and thus the number of choices, it remained unclear whether budget compensation has a trivial effect on demand elasticity by simply sampling from a different total number of choices or has a direct effect on consumers' sequential choice structure. If the budget context independently changes choices between commodities over and above price effects, this should become apparent when demand elasticity is assessed over choice sets of any reasonable size that are matched in choice opportunities between budget conditions. To gain more detailed insight in the sequential choice dynamics underlying differences in demand elasticity between budget conditions, we trained N=8 rat consumers to spend a daily budget by making a number of nosepokes to obtain two liquid commodities under different price regimes, in sessions with and without budget compensation. We confirmed that demand elasticity for both commodities differed between compensated and uncompensated budget conditions, also when the number of choices considered was matched, and showed that these elasticity differences emerge early in the sessions. These differences in demand elasticity were driven by a higher choice rate and an increased reselection bias for the preferred commodity in compensated compared to uncompensated budget conditions, suggesting a budget context effect on relative valuation.
Decision-Making, Bias
Encyclopedia of Computational Neuroscience, 2015
Pro-sociality, i.e., the preference for outcomes that produce benefits for other individuals,
is ... more Pro-sociality, i.e., the preference for outcomes that produce benefits for other individuals,
is ubiquitous in humans. Recently, cross-species comparisons of social behavior have
offered important new insights into the evolution of pro-sociality. Here, we present
a rodent analog of the Pro-social Choice Task that controls strategic components,
de-confounds other-regarding choice motives from the animals’ natural tendencies to
maximize own food access and directly tests the effect of social context on choice
allocation. We trained pairs of rats—an actor and a partner rat—in a double T-maze task
where actors decided between two alternatives only differing in the reward delivered
to the partner. The “own reward” choice yielded a reward only accessible to the actor
whereas the “both reward” choice produced an additional reward for a partner (partner
condition) or an inanimate toy (toy Condition), located in an adjacent compartment. We
found that actors chose “both reward” at levels above chance and more often in the
partner than in the toy condition. Moreover, we show that this choice pattern adapts to
the current social context and that the observed behavior is stable over time
Choice Behavior
Encyclopedia of Computational Neuroscience, 2013
Decision Making, Bias
Encyclopedia of Computational Neuroscience, 2013
Journal of Neuroscience, Jan 8, 2014
Cross-frequency interactions between oscillations in local field potentials (LFPs) are thought to... more Cross-frequency interactions between oscillations in local field potentials (LFPs) are thought to support communication between brain structures by temporally coordinating neural activity. It is unknown, however, whether such interactions differentiate between different levels of performance in decision-making tasks. Here, we investigated theta (4–12 Hz) to gamma (30–100 Hz) phase-amplitude coupling in LFP recordings from rat orbitofrontal cortex. Across subsequent periods of a task in which rats learned to discriminate two odors associated with positive and negative outcomes, theta-to-gamma phase-amplitude coupling (PAC) was highest during the odor-sampling task period that preceded a Go/NoGo decision. This task-dependent modulation could not be explained by changes in oscillatory power and appeared to be time-locked to odor onset, not to the timing of the behavioral response. We found that PAC strength during odor sampling correlated with learning, as indexed by improved performance across trials. Moreover, this increase in PAC magnitude was apparent only on trials with correct Go and NoGo decisions, but not incorrect Go decisions. In addition, we found that PAC preferred coupling phase showed consistency over sessions only for correct, but not incorrect trials.
In conclusion, orbitofrontal cortex theta-gamma PAC strength differentiates between different levels of performance in an olfactory decision-making task and may play a role in the generation and utilization of stimulus-based outcome predictions, necessary for adaptive decision-making.
Neuron, Nov 21, 2012
Neural activity in orbitofrontal cortex has been linked to flexible representations of stimulus-o... more Neural activity in orbitofrontal cortex has been linked to flexible representations of stimulus-outcome associations. Such value representations are known to emerge with learning, but the neural mechanisms supporting this phenomenon are not well understood. Here, we provide evidence for a causal role for NMDA receptors (NMDARs) in mediating spike pattern discriminability, neural plasticity, and rhythmic synchronization in relation to evaluative stimulus processing and decision making. Using tetrodes, single-unit spike trains and local field potentials were recorded during local, unilateral perfusion of an NMDAR blocker in rat OFC. In the absence of behavioral effects, NMDAR blockade severely hampered outcome-selective spike pattern formation to olfactory cues, relative to control perfusions. Moreover, NMDAR blockade shifted local rhythmic synchronization to higher frequencies and degraded its linkage to stimulus-outcome selective coding. These results demonstrate the importance of NMDARs for cue-outcome associative coding in OFC during learning and illustrate how NMDAR blockade disrupts network dynamics.
Frontiers in Neuroscience, 2012
It has been widely recognized that most decisions are made in a social context, and that these co... more It has been widely recognized that most decisions are made in a social context, and that these contexts do influence decisionmaking. The questions remains whether this influence is restricted to humans or primates, or whether this is a more general theme in animal decision-making. Social foraging theory predicts that an animal's foraging choices are not only influenced by the balance in the rate of food intake versus the effort invested, but also by the presence of conspecifics. In two related papers, Ogura and Matsushima (2011) and Amita and Matsushima (2011) report that social manipulations in chicks did influence reward-related motivation, but not choice allocation, suggesting that at least chicks "keep their cool" in a competitive social context. While a social context provides an example of an uncertain environment, uncertainty about future (foraging) outcomes has been traditionally operationalized as risk (uncertainty with known probabilities) and ambiguity (uncertainty about probabilities). Burke and Tobler (2011) review existing data on the neural coding of risk and ambiguity, suggesting largely independent coding of these two aspects of uncertainty that influence human and animal decision-making. Adding new experimental data, Hayden et al. (2010) contributed their latest findings on decisions under risk and ambiguity in monkeys. They show that macaques, that are usually risk-seeking display aversion to ambiguity -much like humans in a closely matched experiment with volunteers. The same authors also report the results from a single unit recording study in monkey posterior cingulate cortex (CGp, Heilbronner et al., 2011). Their results challenge the notion that this area tracks subjective value with single unit and population firing rates, as reported earlier. They show that CGp firing rates do not necessarily track the subjective value of options, as inferred from choice data, but rather are best explained by the deviation of the chosen option from a non-risky, non-delayed "standard" option across decision contexts. This deviation, which they dub "decision salience," could be an attentional signal important for modulation of learning from outcomes. It remains to be seen whether such a neural signal exist in other species.
Annals of the New York Academy of Sciences, 2011
The orbitofrontal cortex has been implicated in the prediction of valuable outcomes based on envi... more The orbitofrontal cortex has been implicated in the prediction of valuable outcomes based on environmental stimuli. However, it remains unknown how it represents outcome-predictive information at the population level, and how it provides temporal structure to such representations. Here, we pay attention especially to the population coding of probabilistic reward, and to the importance of orbitofrontal theta- and gamma-band rhythmicity in relation to target areas. When rats learned to associate odors to food outcome with variable likelihood, we found single-cell and population coding of reward probability, but not uncertainty. In related experiments, reward anticipation correlated to firing activity locking to theta-band oscillations. In contrast, gamma-band activity was associated with a firing-rate suppression of neurons that was most active during goal-directed movement. Orbitofrontal coding of outcome-relevant parameters appears bound to all relevant temporal phases of behavioral tasks, has a distributed nature, and is temporally structured according to multiple modes of rhythmicity.
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Papers by Marijn van Wingerden
is ubiquitous in humans. Recently, cross-species comparisons of social behavior have
offered important new insights into the evolution of pro-sociality. Here, we present
a rodent analog of the Pro-social Choice Task that controls strategic components,
de-confounds other-regarding choice motives from the animals’ natural tendencies to
maximize own food access and directly tests the effect of social context on choice
allocation. We trained pairs of rats—an actor and a partner rat—in a double T-maze task
where actors decided between two alternatives only differing in the reward delivered
to the partner. The “own reward” choice yielded a reward only accessible to the actor
whereas the “both reward” choice produced an additional reward for a partner (partner
condition) or an inanimate toy (toy Condition), located in an adjacent compartment. We
found that actors chose “both reward” at levels above chance and more often in the
partner than in the toy condition. Moreover, we show that this choice pattern adapts to
the current social context and that the observed behavior is stable over time
In conclusion, orbitofrontal cortex theta-gamma PAC strength differentiates between different levels of performance in an olfactory decision-making task and may play a role in the generation and utilization of stimulus-based outcome predictions, necessary for adaptive decision-making.