The late positive potential indexes a role for emotion during learning of trust from eye-gaze cues. : The LPP and learning of trust from gaze

Gaze direction perception triggers rapid visuospatial orienting to the location observed by others. When this is congruent with the location of a target, reaction times are faster than when incongruent. Functional magnetic resonance imaging studies suggest that the non-joint attention induced by incongruent cues are experienced as more emotionally negative and this could relate to less favorable trust judgments of the faces when gaze-cues are contingent with identity. Here, we provide further support for these findings using time-resolved event related potentials. In addition to replicating the effects of identity-contingent gaze-cues on reaction times and trust judgments, we discovered that the emotion-related late positive potential increased across blocks to incongruent compared to congruent faces before, during and after the gaze-cue, suggesting both learning and retrieval of emotion states associated with the face. We also discovered that the face-recognition-related N250 component appeared to localize to sources in anterior temporal areas. Our findings provide unique electrophysiological evidence for the role of emotion in learning trust from gaze-cues, suggesting that the retrieval of face evaluations during interaction may take around 1000 ms and that the N250 originates from anterior temporal face patches

Incidental learning of trust from eye-gaze: Effects of race and facial trustworthiness

Humans rapidly make inferences about individuals’ trustworthiness on the basis of their facial features and perceived group membership. We examine whether incidental learning about trust from shifts in gaze direction is influenced by these facial features. To do so, we examined two types of face category: the race of the face and the initial trustworthiness of the face based on physical appearance. We find that cueing of attention by eye-gaze is unaffected by race or initial levels of trust, whereas incidental learning of trust from gaze behaviour is selectively influenced. That is, learning of trust is reduced for other race faces, as predicted by reduced abilities to identify members of other races (Experiment 1). In contrast, converging findings from an independently gathered set of data showed that the initial trustworthiness of faces did not influence learning of trust (Experiment 2). These results show that learning about the behaviour of other race faces is poorer than for own-race faces, but that this cannot be explained by differences in the perceived trustworthiness of different groups

The role of emotion in the learning of trustworthiness from eye-gaze : Evidence from facial electromyography.

When perception of gaze direction is congruent with the location of a target, attention is facilitated and responses are faster compared to when incongruent. Faces that consistently gaze congruently are also judged trustworthier than faces that consistently gaze incongruently. However, it’s unclear how gaze-cues elicit changes in trust. We measured facial electromyography (EMG) during an identity-contingent gaze-cueing task to examine whether embodied emotional reactions to gaze-cues mediate trust learning. Gaze-cueing effects were found to be equivalent regardless of whether participants showed learning of trust in the expected direction or did not. In contrast, we found distinctly different patterns of EMG activity in these two populations. In a further experiment we showed the learning effects were specific to viewing faces, as no changes in liking were detected when viewing arrows that evoked similar attentional orienting responses. These findings implicate embodied emotion in learning trust from identity-contingent gaze-cueing, possibly due to the social value of shared attention or deception rather than domain-general attentional orienting

Psychophysiological evidence of a role for emotion in the learning of trustworthiness from identity-contingent eye-gaze cues

There is an increasing recognition that emotion influences cognition. This is particularly clear in the domain of social cognition where the perception of social cues is most often a potent source of emotional arousal. One process likely to be influenced by emotion is the forming of face evaluations. Judgements of trustworthiness are particularly important due to the potential costs and benefits of the decision to rely upon another person. Face trustworthiness is modulated by one particular social cue, eye-gaze. In reaction time tasks, when faces gaze away from target objects, incongruently, responses are slower than when faces gaze towards target objects, congruently. Faces that consistently gaze incongruently are also judged less trustworthy than faces that consistently gaze congruently.! In six experiments, we investigated the role of emotion in the learning of trustworthiness from identity-contingent gaze-cues using event-related potentials (ERP) and facial electromyography (EMG), which are sensitive electrophysiological measures of emotion. We found that the learning of trust was paralleled by an increase in the emotionrelated late positive potential (LPP) to incongruent faces across blocks. These findings were further supported by EMG measurements, which showed that corrugator muscle activity related to negative embodied emotional states, was greater to incongruent faces in those participants who showed expected changes in trust ratings. Although effects of gaze-cues on trust were consistent, they were not modulated by extremes in initial trust or priming of emotions elicited by social exclusion. Effects appeared to be due to a special relationship between faces, gaze, emotion and trust as the effects of validity on liking ratings were much weaker or non-existent compared to trust despite evidence of similar emotion-related LPP ERP and EMG activity. The effects also did not generalise to non-social arrow cues. In sum, we conclude that emotion mediates the learning of trust from identity-contingent gaze-cues

The late positive potential indexes a role for emotion during learning of trust from eye-gaze cues.

Soc Neurosci. 2015;10(6):635-50. Work supported by ESRC grant ES/K000012/1 awarded to ST

Incidental learning of trust: Examining the role of emotion and visuomotor fluency.

2016; Journal of Experimental Psychology: Learning, Memory and Cognition. Work supported by ESRC grant ES/K000012/1 awarded to ST

Data files

Data files for Experiments 1 and

Integrated Amygdala, Orbitofrontal and Hippocampal Contributions to Reward and Loss Coding Revealed with Human Intracranial EEG.

Neurophysiological work in primates and rodents have shown the amygdala plays a central role in reward processing through connectivity with the orbitofrontal cortex (OFC) and hippocampus. However, understanding the role of oscillations in each region and their connectivity in different stages of reward processing in humans has been hampered by limitations with noninvasive methods such as poor spatial and temporal resolution. To overcome these limitations, we recorded local field potentials (LFPs) directly from the amygdala, OFC and hippocampus simultaneously in human male and female epilepsy patients performing a monetary incentive delay (MID) task. This allowed us to dissociate electrophysiological activity and connectivity patterns related to the anticipation and receipt of rewards and losses in real time. Anticipation of reward increased high-frequency gamma (HFG; 60-250 Hz) activity in the hippocampus and theta band (4-8 Hz) synchronization between amygdala and OFC, suggesting roles in memory and motivation. During receipt, HFG in the amygdala was involved in outcome value coding, the OFC cue context-specific outcome value comparison and the hippocampus reward coding. Receipt of loss decreased amygdala-hippocampus theta and increased amygdala-OFC HFG amplitude coupling which coincided with subsequent adjustments in behavior. Increased HFG synchronization between the amygdala and hippocampus during reward receipt suggested encoding of reward information into memory for reinstatement during anticipation. These findings extend what is known about the primate brain to humans, showing key spectrotemporal coding and communication dynamics for reward and punishment related processes which could serve as more precise targets for neuromodulation to establish causality and potential therapeutic applications.SIGNIFICANCE STATEMENT Dysfunctional reward processing contributes to many psychiatric disorders. Neurophysiological work in primates has shown the amygdala, orbitofrontal cortex (OFC), and hippocampus play a synergistic role in reward processing. However, because of limitations with noninvasive imaging, it is unclear whether the same interactions occur in humans and what oscillatory mechanisms underpin them. We addressed this issue by recording local field potentials (LFPs) from all three regions in human epilepsy patients during monetary reward processing. There was increased amygdala-OFC high-frequency coupling when losing money which coincided with subsequent adjustments in behavior. In contrast, increased amygdala-hippocampus high-frequency phase-locking suggested a role in reward memory. The findings highlight amygdala networks for reward and punishment processes that could act as more precise neuromodulation targets to treat psychiatric disorders.Natural Science Foundation of China grant (81771482) to BMS. SJTU Trans-med Awards Research (2019015) to BMS. Shanghai Clinical Research Centre for Mental Health (19MC191100) to BMS. Medical Research Council Senior Clinical Fellowship (Grant No. MR/P008747/1) to VV