Gregory S. Berns

A Neural Basis for Social Cooperation

Cooperation based on reciprocal altruism has evolved in only a small number of species, yet it constitutes the core behavioral principle of human social life. The iterated Prisoners Dilemma Game has been used to model this form of cooperation. We used fMRI to scan 36 women as they played an iterated Prisoners Dilemma Game with another woman to investigate the neurobiological basis of cooperative social behavior. Mutual cooperation was associated with consistent activation in brain areas that have been linked with reward processing: nucleus accumbens, the caudate nucleus, ventromedial frontal/orbitofrontal cortex, and rostral anterior cingulate cortex. We propose that activation of this neural network positively reinforces reciprocal altruism, thereby motivating subjects to resist the temptation to selfishly accept but not reciprocate favors.

Neural economics and the biological substrates of valuation

A recent flurry of neuroimaging and decision-making experiments in humans, when combined with single-unit data from orbitofrontal cortex, suggests major additions to current models of reward processing. We review these data and models and use them to develop a specific computational relationship between the value of a predictor and the future rewards or punishments that it promises. The resulting computational model, the predictor-valuation model (PVM), is shown to anticipate a class of single-unit neural responses in orbitofrontal and striatal neurons. The model also suggests how neural responses in the orbitofrontal-striatal circuit may support the conversion of disparate types of future rewards into a kind of internal currency, that is, a common scale used to compare the valuation of future behavioral acts or stimuli.

Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum

Functional MRI experiments in human subjects strongly suggest that the striatum participates in processing information about the predictability of rewarding stimuli. However, stimuli can be unpredictable in character (what stimulus arrives next), unpredictable in time (when the stimulus arrives), and unpredictable in amount (how much arrives). These variables have not been dissociated in previous imaging work in humans, thus conflating possible interpretations of the kinds of expectation errors driving the measured brain responses. Using a passive conditioning task and fMRI in human subjects, we show that positive and negative prediction errors in reward delivery time correlate with BOLD changes in human striatum, with the strongest activation lateralized to the left putamen. For the negative prediction error, the brain response was elicited by expectations only and not by stimuli presented directly; that is, we measured the brain response to nothing delivered (juice expected but not delivered) contrasted with nothing delivered (nothing expected).

Activity in human ventral striatum locked to errors of reward prediction.

The mesolimbic dopaminergic system has long been known to be involved in the processing of rewarding stimuli, although recent evidence from animal research has suggested a more specific role of signaling errors in the prediction of rewards. We tested this hypothesis in humans, using functional magnetic resonance imaging (fMRI) and an operant conditioning paradigm for the discrete delivery of small quantities of fruit juice, along with a control experiment in which juice was substituted with a neutral visual stimulus. A local estimation of the activity in the ventral striatum showed a significant differentiation when the juice was withheld at the expected time of delivery; this finding was not replicated in the case of visual stimulation, providing evidence for time-locked processing of reward prediction errors in human ventral striatum.

Neuromarketing: the hope and hype of neuroimaging in business

The application of neuroimaging methods to product marketing — neuromarketing — has recently gained considerable popularity. We propose that there are two main reasons for this trend. First, the possibility that neuroimaging will become cheaper and faster than other marketing methods; and second, the hope that neuroimaging will provide marketers with information that is not obtainable through conventional marketing methods. Although neuroimaging is unlikely to be cheaper than other tools in the near future, there is growing evidence that it may provide hidden information about the consumer experience. The most promising application of neuroimaging methods to marketing may come before a product is even released — when it is just an idea being developed.

Human Striatal Responses to Monetary Reward Depend On Saliency

While the striatum has been implicated in reward processing, an alternative view contends that the striatum processes salient events in general. Using fMRI, we investigated human striatal responses to monetary reward while modulating the saliency surrounding its receipt. Money was maximally salient when its receipt depended on a correct response (active) and minimally salient when its receipt was completely independent of the task (passive). The saliency manipulation was confirmed by skin conductance responses and subjective ratings of the stimuli. Significant caudate and nucleus accumbens activations occurred following the active compared to passive money. Such activations were attributed to saliency rather than the motor requirement associated with the active money because striatal activations were not observed when the money was replaced by inconsequential, nonrewarding stimuli. The present study provides evidence that the striatums role in reward processing is dependent on the saliency associated with reward, rather than value or hedonic feelings.

Intertemporal choice – toward an integrative framework

Intertemporal choices are decisions with consequences that play out over time. These choices range from the prosaic--how much food to eat at a meal--to life-changing decisions about education, marriage, fertility, health behaviors and savings. Intertemporal preferences also affect policy debates about long-run challenges, such as global warming. Historically, it was assumed that delayed rewards were discounted at a constant rate over time. Recent theoretical and empirical advances from economic, psychological and neuroscience perspectives, however, have revealed a more complex account of how individuals make intertemporal decisions. We review and integrate these advances. We emphasize three different, occasionally competing, mechanisms that are implemented in the brain: representation, anticipation and self-control.

A Computational Model of How the Basal Ganglia Produce Sequences

We propose a systems-level computational model of the basal ganglia based closely on known anatomy and physiology. First, we assume that the thalamic targets, which relay ascending information to cortical action and planning areas, are tonically inhibited by the basal ganglia. Second, we assume that the output stage of the basal ganglia, the internal segment of the globus pallidus (GPi), selects a single action from several competing actions via lateral interactions. Third, we propose that a form of local working memory exists in the form of reciprocal connections between the external globus pallidus (GPe) and the subthalamic nucleus (STN). As a test of the model, the system was trained to learn a sequence of states that required the context of previous actions. The striatum, which was assumed to represent a conjunction of cortical states, directly selected the action in the GP during training. The STN-to-GP connection strengths were modified by an associative learning rule and came to encode the sequence after 20 to 40 iterations through the sequence. Subsequently, the system automatically reproduced the sequence when cued to the first action. The behavior of the model was found to be sensitive to the ratio of the striatal-nigral learning rate to the STN-GP learning rate. Additionally, the degree of striatal inhibition of the globus pallidus had a significant influence on both learning and the ability to select an action. Low learning rates, which would be hypothesized to reflect low levels of dopamine, as in Parkinsons disease, led to slow acquisition of contextual information. However, this could be partially offset by modeling a lesion of the globus pallidus that resulted in an increase in the gain of the STN units. The parameter sensitivity of the model is discussed within the framework of existing behavioral and lesion data.

Neurobiological correlates of social conformity and independence during mental rotation

BACKGROUND When individual judgment conflicts with a group, the individual will often conform his judgment to that of the group. Conformity might arise at an executive level of decision making, or it might arise because the social setting alters the individuals perception of the world. METHODS We used functional magnetic resonance imaging and a task of mental rotation in the context of peer pressure to investigate the neural basis of individualistic and conforming behavior in the face of wrong information. RESULTS Conformity was associated with functional changes in an occipital-parietal network, especially when the wrong information originated from other people. Independence was associated with increased amygdala and caudate activity, findings consistent with the assumptions of social norm theory about the behavioral saliency of standing alone. CONCLUSIONS These findings provide the first biological evidence for the involvement of perceptual and emotional processes during social conformity.

Anterior cingulate activation and error processing during interferon-alpha treatment.

BACKGROUND There has been increasing interest in the role of immunologic processes, notably cytokines, in the development of behavioral alterations, especially in medically ill patients. Interferon (IFN)-alpha is notorious for causing behavioral symptoms, including depression, fatigue, and cognitive dysfunction, and has been used to investigate the effects of cytokines on the brain. METHODS In the present study we assessed the effects of low-dose IFN-alpha on brain activity, using functional magnetic resonance imaging during a task of visuospatial attention in patients infected with hepatitis C virus (HCV). RESULTS Despite endorsing symptoms of impaired concentration and fatigue, IFN-alpha-treated patients (n = 10) exhibited task performance and activation of parietal and occipital brain regions similar to that seen in HCV-infected control subjects (n = 11). Interestingly, however, in contrast to control subjects, IFN-alpha-treated patients exhibited significant activation in the dorsal part of the anterior cingulate cortex (ACC), which highly correlated with the number of task-related errors. No such correlation was found in control subjects. CONCLUSIONS Consistent with the role of the ACC in conflict monitoring, ACC activation during IFN-alpha administration suggests that cytokines might increase processing conflict or reduce the threshold for conflict detection, thereby signaling the need to exert greater mental effort to maintain performance. Such alterations in ACC activity might in turn contribute to cytokine-induced behavioral changes.