Neural Correlates of Social Target Value in Macaque Parietal Cortex

Klein, Jeffrey T.; Deaner, Robert O.; Platt, Michael L.

doi:10.1016/j.cub.2008.02.047

Cited by 106 publications

(111 citation statements)

References 30 publications

(35 reference statements)

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“…These results are consistent with LIP receiving feed-forward information from successively higher levels of the visual system, with directional social gaze signals arriving relatively late. These findings are also consistent with the idea that LIP mediates both social salience assessment (46) and oculomotor reward contingencies related to task demands (42). We speculate that gaze-cue enhanced neurons signal the increased value of acquiring information about regions of space where other monkeys are looking.…”

Section: Resultssupporting

confidence: 90%

“…To permit electrophysiological recordings, macaques were additionally implanted with a stainless steel recording chamber (Crist) over posterior parietal cortex (LIP) (46,48). Before each session, the chamber was aseptically opened, rinsed thoroughly with sterile saline, and fit with a plastic grid (Crist) (75).…”

Section: Methodsmentioning

confidence: 99%

“…Data were recorded by custom software (http://www.ryklinsoftware.com) and imported into Matlab for further analysis by custom scripts. All surgical procedures were performed aseptically, followed with appropriate analgesics and antibiotics, and in all other ways followed standard protocols described (5,46). Task.…”

Section: Methodsmentioning

confidence: 99%

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Mirroring of attention by neurons in macaque parietal cortex

Shepherd

Klein²,

Deaner³

et al. 2009

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

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Macaques, like humans, rapidly orient their attention in the direction other individuals are looking. Both cortical and subcortical pathways have been proposed as neural mediators of social gaze following, but neither pathway has been characterized electrophysiologically in behaving animals. To address this gap, we recorded the activity of single neurons in the lateral intraparietal area (LIP) of rhesus macaques to determine whether and how this area might contribute to gaze following. A subset of LIP neurons mirrored observed attention by firing both when the subject looked in the preferred direction of the neuron, and when observed monkeys looked in the preferred direction of the neuron, despite the irrelevance of the monkey images to the task. Importantly, the timing of these modulations matched the time course of gaze-following behavior. A second population of neurons was suppressed by social gaze cues, possibly subserving task demands by maintaining fixation on the observed face. These observations suggest that LIP contributes to sharing of observed attention and link mirror representations in parietal cortex to a well studied imitative behavior.gaze following ͉ imitation ͉ joint attention ͉ mirror neurons ͉ shared attention P eople naturally and intuitively share attention with each other. In a laboratory setting, people respond more quickly to targets that are the object of another's attention, even when this social cuing is brief or consistently misleading (1-3). Monkeys' attention also follows the gaze of others (4), and the similar magnitude and time course of gaze following by rhesus macaques and humans (5) implicates shared neural mechanisms. The ability to follow gaze is believed to be an important foundation for theory of mind (6, 7); thus, the neural processes governing gaze following are relevant both to the evolution of social cognition (8-10) and to clinical disorders, such as autism, associated with social attention deficits (11)(12)(13)(14). Although gaze following involves automatic ''mirroring'' of other's mental states, to our knowledge, mirror neurons (15, 16) for visual orienting have not previously been identified.Current evidence suggests that identification of where other individuals are looking is accomplished by neurons along the superior temporal sulcus (STS) (17)(18)(19)(20) (22), as well as the parietal cortex (28). These observations invite the simple hypothesis that gazefollowing behavior is mediated by a relatively straightforward system, beginning with the STS and proceeding directly to the attention-and gaze-control networks. Although intuitively appealing, this model raises several important questions.First, gaze-following behavior fits poorly into existing models of attention (1, 2), which dichotomize the underlying mechanism as either reflexively driven by exogenous stimuli or endogenously guided by internal goals (29, 30). Although there is some evidence that specific neural circuits mediate these processes (31-33), the precise contributions of neurons within different b...

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Section: Resultssupporting

confidence: 90%

Section: Methodsmentioning

confidence: 99%

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Mirroring of attention by neurons in macaque parietal cortex

Shepherd

Klein²,

Deaner³

et al. 2009

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

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111

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“…1B, blue bars), as reported previously (18)(19)(20). Although monkeys spent more time viewing perinea than control stimuli (P < 0.0001), they spent less time viewing the faces of dominant monkeys (P < 0.01), as reported previously (19)(20)(21). Monkeys also responded about 8 ms faster in blocks with dominant faces compared with other blocks [Fig.…”

Section: Resultssupporting

confidence: 86%

Oxytocin blunts social vigilance in the rhesus macaque

Ebitz

Watson

2013

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

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Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.attention | primates | face gaze | neuropeptide

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“…Common scale value coding is a prerequisite for applying Equation 25 to neuronal signals and is seen in orbitofrontal cortex with different liquid rewards (405) and images of body parts (629), in parietal cortex with body part images (279), and in dopamine neurons with different liquid and food rewards (301) (FIGURE 23, B AND D). Neuronal signals reflect the sum of positive and negative values from liquid or food rewards and aversive liquids or air puff punisher in monkey dopamine neurons (FIGURE 11D) (157,160) and anterior cingulate cortex (10), and from odor rewards in human orbitofrontal cortex (190).…”

Section: Equation 25mentioning

confidence: 99%

Neuronal Reward and Decision Signals: From Theories to Data

Schultz

2015

Physiological Reviews

893

765

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LSchultz W. Neuronal Reward and Decision Signals: From Theories to Data. Physiol Rev 95: 853-951, 2015. Published June 24, 2015 doi:10.1152/physrev.00023.2014.-Rewards are crucial objects that induce learning, approach behavior, choices, and emotions. Whereas emotions are difficult to investigate in animals, the learning function is mediated by neuronal reward prediction error signals which implement basic constructs of reinforcement learning theory. These signals are found in dopamine neurons, which emit a global reward signal to striatum and frontal cortex, and in specific neurons in striatum, amygdala, and frontal cortex projecting to select neuronal populations. The approach and choice functions involve subjective value, which is objectively assessed by behavioral choices eliciting internal, subjective reward preferences. Utility is the formal mathematical characterization of subjective value and a prime decision variable in economic choice theory. It is coded as utility prediction error by phasic dopamine responses. Utility can incorporate various influences, including risk, delay, effort, and social interaction. Appropriate for formal decision mechanisms, rewards are coded as object value, action value, difference value, and chosen value by specific neurons. Although all reward, reinforcement, and decision variables are theoretical constructs, their neuronal signals constitute measurable physical implementations and as such confirm the validity of these concepts. The neuronal reward signals provide guidance for behavior while constraining the free will to act.

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Neural Correlates of Social Target Value in Macaque Parietal Cortex

Cited by 106 publications

References 30 publications

Mirroring of attention by neurons in macaque parietal cortex

Mirroring of attention by neurons in macaque parietal cortex

Oxytocin blunts social vigilance in the rhesus macaque

Neuronal Reward and Decision Signals: From Theories to Data

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