Social Information Signaling by Neurons in Primate Striatum

Klein, Jeffrey T.; Platt, Michael L.

doi:10.1016/j.cub.2013.03.022

Cited by 61 publications

(54 citation statements)

References 39 publications

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“…Tracking group members' status serves vital functions supported by valuation regions, such as assigning motivational importance to particular individuals, monitoring and detecting their presence, and signaling they deserve privileged status in attention and decision-making (17,(19)(20)(21)(22). In an experimental demonstration of this principle, rhesus macaques were willing to sacrifice fruit juice to view faces of high-status group members, while requiring overpayment of juice to view low-status monkeys' faces (38).…”

Section: Discussionmentioning

confidence: 99%

“…The observed correlations between target popularity and activity in valuation and social cognition regions confirmed our primary hypotheses, which led to our second question: Do the two systems track popularity in parallel (independently) or serially, with one system assuming a primary role that mediates the popularity-activity relationship for the other? We predicted the valuation system would function as mediator based on the aforementioned literatures in social psychology [i.e., it is highstatus individuals' social importance that motivates others to predict their mental states (25)(26)(27)(28)] and nonhuman primate neurophysiology [i.e., neurons in valuation regions encode social value and signal presence of high-status group members (19)(20)(21)(22)]. To test this prediction, we performed multilevel mediation analyses, assessing whether valuation system activity explains the observed relationship between target popularity and social cognition system activity.…”

Section: And Person Judgment Tasks (See Ref 23 For Review)mentioning

confidence: 99%

“…These densely interconnected regions (13), henceforth referred to collectively as the "valuation system," are consistently implicated in processing the affective value and motivational significance of various stimuli, including other people (13)(14)(15)(16)(17)(18). Although human neuroscience research has yet to investigate sociometric popularity, nonhuman primate researchers have found that neurons in these regions signal group members' dominance rank (19)(20)(21) and proposed that the vmPFC, VS, and amygdala interact to encode, monitor, and signal other individuals' social value (22). If tracking group members' popularity depends on the motivational significance…”

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confidence: 99%

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Neural mechanisms tracking popularity in real-world social networks

Zerubavel

Bearman

Weber

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

102

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Differences in popularity are a key aspect of status in virtually all human groups and shape social interactions within them. Little is known, however, about how we track and neurally represent others' popularity. We addressed this question in two real-world social networks using sociometric methods to quantify popularity. Each group member (perceiver) viewed faces of every other group member (target) while whole-brain functional MRI data were collected. Independent functional localizer tasks were used to identify brain systems supporting affective valuation (ventromedial prefrontal cortex, ventral striatum, amygdala) and social cognition (dorsomedial prefrontal cortex, precuneus, temporoparietal junction), respectively. During the face-viewing task, activity in both types of neural systems tracked targets' sociometric popularity, even when controlling for potential confounds. The target popularity-social cognition system relationship was mediated by valuation system activity, suggesting that observing popular individuals elicits value signals that facilitate understanding their mental states. The target popularity-valuation system relationship was strongest for popular perceivers, suggesting enhanced sensitivity to differences among other group members' popularity. Popular group members also demonstrated greater interpersonal sensitivity by more accurately predicting how their own personalities were perceived by other individuals in the social network. These data offer insights into the mechanisms by which status guides social behavior.social status | fMRI | social network | popularity | social cognition

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Section: Discussionmentioning

confidence: 99%

Section: And Person Judgment Tasks (See Ref 23 For Review)mentioning

confidence: 99%

mentioning

confidence: 99%

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Neural mechanisms tracking popularity in real-world social networks

Zerubavel

Bearman

Weber

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

102

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“…female perineum, high status male face) or a large juice reward, but respond less when the same monkeys choose unpreferred social images (e.g. low status faces) or small juice rewards [76][77][78], consistent with an abstract code for value.…”

Section: Mechanisms Mediating the Evaluation Of Social Partners' Valumentioning

confidence: 99%

Adaptations for social cognition in the primate brain

Platt

Seyfarth

Cheney

2016

Phil. Trans. R. Soc. B

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One contribution of 18 to a theme issue 'The evolution of cooperation based on direct fitness benefits'. Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals' fitness interdependent and the 'free-rider' problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation-often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and nonsocial decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and nonhuman primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.

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“…Single-unit recording studies in non-human primates are beginning to identify different types of neurons in the striatum, OFC and ACC that may selectively encode social versus non-social aspects of rewards. For example, different types of neurons in the striatum have been found to respond to social (images of conspecifics) or non-social (juice) rewards 104 or to be involved in signalling either when a reward was given or when this reward was due to the action of the monkey or a conspecific 105 . Another study found that neurons in the macaque OFC mainly encoded rewards given to the monkey himself, whereas neurons in a subportion of the ACC encoded rewards received by another monkey 106 .…”

Section: Is Social Neural Valuation Distinct?mentioning

confidence: 99%

The neurobiology of rewards and values in social decision making

2014

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Of all the decisions in your life, which were the most important? Chances are high that many of them had a social component, be it when deciding about others (for example, whether to marry someone), for others (for example, which school to send your child to) or jointly with others (for example, whether to buy a house with your partner). Pathological changes specifically in the social aspects of decision making are pervasive in many psychiatric 1 and neurological 2 disorders and can have devastating consequences for individual and collective welfare. A good understanding of the neural basis of social decision making is thus an important aim of scientists in many disciplines, from basic neuroscience to medicine, psychology and economics.The neural mechanisms underlying social and nonsocial types of choices have traditionally been examined from different theoretical angles. In studies of non-social choices (for example, purchasing decisions), researchers have often focused on neural value computations associated with the rewarding properties of the choice options 3,4 . On the basis of this research, several brain structures have been proposed as elements of a brain valuation system (BOX 1). The neural value signals in these structures are thought to represent a 'common currency' for assessing the motivational relevance of all possible stimuli or actions, which is essential for guiding decision making across varying contexts 5,6 . By contrast, researchers studying social decisions have traditionally paid less attention to motivational processes, such as reward and value coding; instead, they have focused on identifying neurocognitive processes that may have uniquely evolved to guide social behaviour 7 . This emphasis on 'social-specific cognition' has identified, for example, that different visual areas seem to be functionally specialized for the perception of faces or bodies 8 and that the dorsomedial prefrontal cortex (dmPFC) and the temporoparietal junction (TPJ) may be specifically involved in representing the intentions, emotions or actions of other people [9][10][11] . The idea of 'social-specific cognition' thus implies that the control of social and non-social behaviour should fundamentally differ in terms of neural architecture and information processing demands 12 . However, this view is challenged by recent findings that social decisions may also draw on value-related brain processes that strongly resemble those seen during non-social decisions. This apparent overlap in neural representations of motivational relevance for social and non-social choices is often taken to implicitly extend the 'common currency' idea to decisions based on social factors. This proposalthat choices in both social and non-social situations are steered by identical neural value computations -therefore questions whether the motivational control of social behaviour requires dedicated neural processes.In this Review, we propose a framework for studying the possible neurobiological links in the motivational control of social...

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Social Information Signaling by Neurons in Primate Striatum

Cited by 61 publications

References 39 publications

Neural mechanisms tracking popularity in real-world social networks

Neural mechanisms tracking popularity in real-world social networks

Adaptations for social cognition in the primate brain

The neurobiology of rewards and values in social decision making

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