Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala

Hoffman, Kari L.; Gothard, Katalin M.; Schmid, Michael C.; Logothetis, Nikos K.

doi:10.1016/j.cub.2007.03.040

Cited by 250 publications

(251 citation statements)

References 46 publications

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“…However, given the copious amounts of anecdotal evidence from humans, and the more recent empirical studies supporting the uncanny valley effect in humans (2, 3), it seems parsimonious to conclude that monkeys are also experiencing at least some of the same emotions. To support this notion, future experiments could incorporate somatic markers, such as skin conductance responses, pupil dilation, or facial electromyography, to measure the emotional responses of monkeys to the differently rendered faces from monkeys (17)(18)(19)(20). Neurophysiological and neuroimaging approaches could also be illuminating in this regard.…”

Section: Resultsmentioning

confidence: 99%

Monkey visual behavior falls into the uncanny valley

Steckenfinger

Ghazanfar

2009

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

131

126

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Very realistic human-looking robots or computer avatars tend to elicit negative feelings in human observers. This phenomenon is known as the ''uncanny valley'' response. It is hypothesized that this uncanny feeling is because the realistic synthetic characters elicit the concept of ''human,'' but fail to live up to it. That is, this failure generates feelings of unease due to character traits falling outside the expected spectrum of everyday social experience. These unsettling emotions are thought to have an evolutionary origin, but tests of this hypothesis have not been forthcoming. To bridge this gap, we presented monkeys with unrealistic and realistic synthetic monkey faces, as well as real monkey faces, and measured whether they preferred looking at one type versus the others (using looking time as a measure of preference). To our surprise, monkey visual behavior fell into the uncanny valley: They looked longer at real faces and unrealistic synthetic faces than at realistic synthetic faces.animacy ͉ audiovisual speech ͉ avatar ͉ face processing ͉ human robot interaction

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Section: Resultsmentioning

confidence: 99%

Monkey visual behavior falls into the uncanny valley

Steckenfinger

Ghazanfar

2009

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

131

126

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“…However, previous studies have reported various effects of gaze processing in the human amygdala, including enhanced activity to either direct gaze (Kawashima et al, 1999) or averted gaze (Hadjikhani et al, 2008;Staube et al, 2010) or, as in our study, no differential activity for the two gaze directions with static (Wicker et al, 1998) or dynamic stimuli (Pelphrey et al, 2003b;Pelphrey et al, 2004b). Possible explanations for this inconsistency include a low signal-to-noise ratio, since fMRI of subnuclei of the amygdala in monkeys has shown that gaze specific responses are restricted to the central nucleus and the bed nucleus of the stria terminalis (Hoffman et al, 2007); or alternatively, interactions with other experimental factors such as head direction, task instructions, or All values correspond to the number of subjects who exhibited a structural connection between the seed and the target areas, among all 22 volunteers who were scanned. All values correspond to the number of subjects who exhibited a structural connection between the seed and the target areas, among all 22 volunteers who were scanned.…”

Section: Discussionmentioning

confidence: 99%

Processing social aspects of human gaze: A combined fMRI-DTI study

2011

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Human gaze is a critical social cue that can reveal intentions and dispositions of others. The right posterior superior temporal sulcus (pSTS) is thought to be critically involved in processing eye gaze information. We combined diffusion tensor imaging (DTI) and functional magnetic resonance imaging (fMRI) to identify direct neural connections of right pSTS and to determine how these connections are modulated by the social significance of perceived gaze shifts. Participants saw faces with direct or averted gaze during event-related fMRI. Half of these faces remained static, and half displayed a dynamic gaze shift either towards or away from the subject. Social attention (dynamic gaze shifts towards the observer) not only increased activity in right pSTS, but also its functional connectivity with the right anterior insula (aIns) and right fusiform gyrus (FG). However, direct fiber connections from pSTS were demonstrated by DTI for the right aIns, but not the right FG. Moreover, the right FG responded to eye motion irrespective of direction and social significance; whereas the right aIns was selectively sensitive to social significance (i.e. gaze shifts towards the observer), but not generally to eye motion. We conclude that the social aspects of mutual gaze contact are processed by direct fiber pathways between right pSTS and right aIns; whereas increased connectivity with FG could reflect an enhanced perceptual analysis of changing facial features in dynamic gaze conditions and involves indirect fiber pathways with pSTS, perhaps via motion-selective regions in middle temporal (MT) gyrus that exhibited strong white-matter connections with both pSTS and FG and could thus provide inputs to these two areas.

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“…Subjects with amygdala damage fail to recognize fear faces (5), although there is now a consensus that the amygdala is involved in processing many emotions from faces, not just fear (11). Electrophysiological recordings in monkeys have found single neurons that respond not only to faces as such (12,13), but also to face identities, facial expressions, and gaze directions (14,15). Single neurons in the human amygdala discriminate faces from inanimate objects (10).…”

mentioning

confidence: 99%

Neurons in the human amygdala selective for perceived emotion

Wang

Tudusciuc

Mamelak³

et al. 2014

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

127

114

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The human amygdala plays a key role in recognizing facial emotions and neurons in the monkey and human amygdala respond to the emotional expression of faces. However, it remains unknown whether these responses are driven primarily by properties of the stimulus or by the perceptual judgments of the perceiver. We investigated these questions by recording from over 200 single neurons in the amygdalae of 7 neurosurgical patients with implanted depth electrodes. We presented degraded fear and happy faces and asked subjects to discriminate their emotion by button press. During trials where subjects responded correctly, we found neurons that distinguished fear vs. happy emotions as expressed by the displayed faces. During incorrect trials, these neurons indicated the patients' subjective judgment. Additional analysis revealed that, on average, all neuronal responses were modulated most by increases or decreases in response to happy faces, and driven predominantly by judgments about the eye region of the face stimuli. Following the same analyses, we showed that hippocampal neurons, unlike amygdala neurons, only encoded emotions but not subjective judgment. Our results suggest that the amygdala specifically encodes the subjective judgment of emotional faces, but that it plays less of a role in simply encoding aspects of the image array. The conscious percept of the emotion shown in a face may thus arise from interactions between the amygdala and its connections within a distributed cortical network, a scheme also consistent with the long response latencies observed in human amygdala recordings.human single unit | medial temporal lobe | limbic system | hippocampus | intracranial

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Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala

Cited by 250 publications

References 46 publications

Monkey visual behavior falls into the uncanny valley

Monkey visual behavior falls into the uncanny valley

Processing social aspects of human gaze: A combined fMRI-DTI study

Neurons in the human amygdala selective for perceived emotion

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