The anterior cingulate cortex (ACC) is implicated in a broad range of behaviors and cognitive processes, but it has been unclear what contribution, if any, the ACC makes to social behavior. We argue ...that anatomical and functional evidence suggests that a specific sub-region of ACC—in the gyrus (ACCg)—plays a crucial role in processing social information. We propose that the computational properties of the ACCg support a contribution to social cognition by estimating how motivated other individuals are and dynamically updating those estimates when further evidence suggests they have been erroneous. Notably this model, based on vicarious motivation and error processing, provides a unified account of neurophysiological and neuroimaging evidence that the ACCg is sensitive to costs, benefits, and errors during social interactions. Furthermore, it makes specific, testable predictions about a key mechanism that may underpin variability in socio-cognitive abilities in health and disease.
•The anterior cingulate gyrus (ACCg) mainly signals other-oriented information•The ACCg responds to others’ motivation and prediction errors•ACCg variability may lead to variability in social cognition in health and disease•A computational framework is proposed accounting for ACCg social responses
Apps et al. review specialized properties of the anterior cingulate gyrus in social cognition and put forward a computational account of how the motivation of other agents is estimated in the anterior cingulate gyrus of human and non-human primates.
The causal role of an area within a neural network can be determined by interfering with its activity and measuring the impact. Many current reversible manipulation techniques have limitations ...preventing their application, particularly in deep areas of the primate brain. Here, we demonstrate that a focused transcranial ultrasound stimulation (TUS) protocol impacts activity even in deep brain areas: a subcortical brain structure, the amygdala (experiment 1), and a deep cortical region, the anterior cingulate cortex (ACC, experiment 2), in macaques. TUS neuromodulatory effects were measured by examining relationships between activity in each area and the rest of the brain using functional magnetic resonance imaging (fMRI). In control conditions without sonication, activity in a given area is related to activity in interconnected regions, but such relationships are reduced after sonication, specifically for the targeted areas. Dissociable and focal effects on neural activity could not be explained by auditory confounds.
•Ultrasound stimulation exerts regionally specific neural effects in primates•It can be used to alter activity even in subcortical and deep cortical areas•After stimulation, activity in a brain area is less related to that of its network•The effect lasted for more than 1 h and was not mediated by auditory confounds
Ultrasound can be used to modulate activity in deep brain areas. After stimulation, activity in the targeted brain area becomes less coupled to its network. Effects are specific to the stimulation site, long-lasting, and not due to auditory confounds.
Neural Mechanisms of Foraging Kolling, Nils; Behrens, Timothy E. J.; Mars, Rogier B. ...
Science (American Association for the Advancement of Science),
04/2012, Volume:
336, Issue:
6077
Journal Article
Peer reviewed
Open access
Behavioral economic studies involving limited numbers of choices have provided key insights into neural decision-making mechanisms. By contrast, animals' foraging choices arise in the context of ...sequences of encounters with prey or food. On each encounter, the animal chooses whether to engage or, if the environment is sufficiently rich, to search elsewhere. The cost of foraging is also critical. We demonstrate that humans can alternate between two modes of choice, comparative decision-making and foraging, depending on distinct neural mechanisms in ventromedial prefrontal cortex (vmPFC) and anterior cingulate cortex (ACC) using distinct reference frames; in ACC, choice variables are represented in invariant reference to foraging or searching for alternatives. Whereas vmPFC encodes values of specific well-defined options, ACC encodes the average value of the foraging environment and cost of foraging.
Reward-guided decision-making and learning depends on distributed neural circuits with many components. Here we focus on recent evidence that suggests four frontal lobe regions make distinct ...contributions to reward-guided learning and decision-making: the lateral orbitofrontal cortex, the ventromedial prefrontal cortex and adjacent medial orbitofrontal cortex, anterior cingulate cortex, and the anterior lateral prefrontal cortex. We attempt to identify common themes in experiments with human participants and with animal models, which suggest roles that the areas play in learning about reward associations, selecting reward goals, choosing actions to obtain reward, and monitoring the potential value of switching to alternative courses of action.
Sometimes when a choice is made, the outcome is not guaranteed and there is only a probability of its occurrence. Each individual’s attitude to probability, sometimes called risk proneness or ...aversion, has been assumed to be static. Behavioral ecological studies, however, suggest such attitudes are dynamically modulated by the context an organism finds itself in; in some cases, it may be optimal to pursue actions with a low probability of success but which are associated with potentially large gains. We show that human subjects rapidly adapt their use of probability as a function of current resources, goals, and opportunities for further foraging. We demonstrate that dorsal anterior cingulate cortex (dACC) carries signals indexing the pressure to pursue unlikely choices and signals related to the taking of such choices. We show that dACC exerts this control over behavior when it, rather than ventromedial prefrontal cortex, interacts with posterior cingulate cortex.
•Against common belief, risk preference is not fixed but is dynamically updated•Environments exert varying “risk pressure” tracked by ACC•Risk-related values and behavior are then regulated by ACC•Two mechanisms regulate competition for control of behavior between ACC and vmPFC
The propensity to take risks has been considered a fixed personality trait. By contrast, Kolling et al. show that people modulate their degree of risk taking from moment to moment and that this ability is related to a suite of signals in the anterior cingulate cortex.
Controversy surrounds the role of the temporoparietal junction (TPJ) area of the human brain. Although TPJ has been implicated both in reorienting of attention and social cognition, it is still ...unclear whether these functions have the same neural basis. Indeed, whether TPJ is a precisely identifiable cortical region or a cluster of subregions with separate functions is still a matter of debate. Here, we examined the structural and functional connectivity of TPJ, testing whether TPJ is a unitary area with a heterogeneous functional connectivity profile or a conglomerate of regions with distinctive connectivity. Diffusion-weighted imaging tractrography-based parcellation identified 3 separate regions in TPJ. Resting-state functional connectivity was then used to establish which cortical networks each of these subregions participates in. A dorsal cluster in the middle part of the inferior parietal lobule showed resting-state functional connectivity with, among other areas, lateral anterior prefrontal cortex. Ventrally, an anterior TPJ cluster interacted with ventral prefrontal cortex and anterior insula, while a posterior TPJ cluster interacted with posterior cingulate, temporal pole, and anterior medial prefrontal cortex. These results indicate that TPJ can be subdivided into subregions on the basis of its structural and functional connectivity.
Computation of Social Behavior Behrens, Timothy E.J; Hunt, Laurence T; Rushworth, Matthew F.S
Science (American Association for the Advancement of Science),
05/2009, Volume:
324, Issue:
5931
Journal Article
Peer reviewed
Neuroscientists are beginning to advance explanations of social behavior in terms of underlying brain mechanisms. Two distinct networks of brain regions have come to the fore. The first involves ...brain regions that are concerned with learning about reward and reinforcement. These same reward-related brain areas also mediate preferences that are social in nature even when no direct reward is expected. The second network focuses on regions active when a person must make estimates of another person's intentions. However, it has been difficult to determine the precise roles of individual brain regions within these networks or how activities in the two networks relate to one another. Some recent studies of reward-guided behavior have described brain activity in terms of formal mathematical models; these models can be extended to describe mechanisms that underlie complex social exchange. Such a mathematical formalism defines explicit mechanistic hypotheses about internal computations underlying regional brain activity, provides a framework in which to relate different types of activity and understand their contributions to behavior, and prescribes strategies for performing experiments under strong control.
Activity in a network of areas spanning the superior temporal sulcus, dorsomedial frontal cortex, and anterior cingulate cortex is concerned with how nonhuman primates negotiate the social worlds in ...which they live. Central aspects of these circuits are retained in humans. Activity in these areas codes for primates' interactions with one another, their attempts to find out about one another, and their attempts to prevent others from finding out too much about themselves. Moreover, important features of the social world, such as dominance status, cooperation, and competition, modulate activity in these areas. We consider the degree to which activity in these regions is simply encoding an individual's own actions and choices or whether this activity is especially and specifically concerned with social cognition. Recent advances in comparative anatomy and computational modeling may help us to gain deeper insights into the nature and boundaries of primate social cognition.
Comparative neuroscience is entering the era of big data. New high-throughput methods and data-sharing initiatives have resulted in the availability of large, digital data sets containing many types ...of data from ever more species. Here, we present a framework for exploiting the new possibilities offered. The multimodality of the data allows vertical translations, which are comparisons of different aspects of brain organization within a single species and across scales. Horizontal translations compare particular aspects of brain organization across species, often by building abstract feature spaces. Combining vertical and horizontal translations allows for more sophisticated comparisons, including relating principles of brain organization across species by contrasting horizontal translations, and for making formal predictions of unobtainable data based on observed results in a model species.
Associative learning of social value Behrens, Timothy E. J; Hunt, Laurence T; Woolrich, Mark W ...
Nature,
11/2008, Volume:
456, Issue:
7219
Journal Article
Peer reviewed
Open access
Our decisions are guided by information learnt from our environment. This information may come via personal experiences of reward, but also from the behaviour of social partners. Social learning is ...widely held to be distinct from other forms of learning in its mechanism and neural implementation; it is often assumed to compete with simpler mechanisms, such as reward-based associative learning, to drive behaviour. Recently, neural signals have been observed during social exchange reminiscent of signals seen in studies of associative learning. Here we demonstrate that social information may be acquired using the same associative processes assumed to underlie reward-based learning. We find that key computational variables for learning in the social and reward domains are processed in a similar fashion, but in parallel neural processing streams. Two neighbouring divisions of the anterior cingulate cortex were central to learning about social and reward-based information, and for determining the extent to which each source of information guides behaviour. When making a decision, however, the information learnt using these parallel streams was combined within ventromedial prefrontal cortex. These findings suggest that human social valuation can be realized by means of the same associative processes previously established for learning other, simpler, features of the environment.
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