Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys

Taubert, Jessica; Flessert, Molly; Wardle, Susan G.; Basile, Benjamin M.; Murphy, Aidan P.; Murray, Elisabeth A.; Ungerleider, Leslie G.

doi:10.1073/pnas.1807245115

Cited by 69 publications

(64 citation statements)

References 52 publications

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“…6). These results are consistent with the findings of previous studies (Emery, 2000;Mosher et al, 2014;Dal Monte et al, 2015;Forcelli et al, 2016;Minxha et al, 2017;Taubert et al, 2018).…”

Section: Discussionsupporting

confidence: 93%

“…While the amygdala is known to mediate threat detection and passive fear responses, it remains unclear if this structure also contributes to controlling eye movements. Some studies have shown that amygdala lesions alter gaze patterns, especially for face images (Dal Monte et al, 2015;Taubert et al, 2018). Other studies have shown that amygdala neurons are spatially selective and encode information about both the location and the motivational significance of visual cues (Peck and Salzman, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Amygdala controls saccade and gaze physically, motivationally, and socially

Maeda

Inoue

Kunimatsu

et al. 2019

Preprint

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Highlights-Central amygdala facilitates contralateral saccades selectively. -Saccade facilitation is related to motivational goals and social interaction. -The amygdala thus controls goal-directed behavior based on emotional contexts. AbstractThe amygdala is uniquely sensitive to emotional events. However, it is not understood whether and how the amygdala uses such emotional signals to control behavior, especially eye movements. We therefore injected muscimol (GABA A agonist) into the central nucleus of amygdala (CeA) in monkeys. This unilateral temporary inactivation suppressed saccades to contralateral but not ipsilateral targets, resulting in longer latencies, hypometric amplitudes, and slower velocity. During free viewing of movies, gaze was distributed mostly in the ipsilateral hemifield. Moreover, CeA inactivation disrupted the tendency of gaze toward social interaction images, which were normally focused on continuously. Conversely, optogenetic stimulation of CeA facilitated saccades to the contralateral side. These findings suggest that CeA controls spatially selective gaze and attention in emotional contexts, and provide a new framework for understanding psychiatric disorders related to amygdala dysfunction.

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“…6). These results are consistent with the findings of previous studies (Emery, 2000;Mosher et al, 2014;Dal Monte et al, 2015;Forcelli et al, 2016;Minxha et al, 2017;Taubert et al, 2018).…”

Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Amygdala controls saccade and gaze physically, motivationally, and socially

Maeda

Inoue

Kunimatsu

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…The fact that human faces and illusory faces are readily decoded from each other in both fMRI and MEG is also indicative of differences in their representation. Overall, this difference is consistent with the interpretation of illusory faces as a quickly resolved error of a broadly tuned face-detection system 2,3 . Thus although illusory faces elicit a face-like response, they are not represented in the same way as human faces within the visual system.…”

Section: Discussionsupporting

confidence: 84%

“…A rapid subcortical route for face detection has been proposed based on multiple lines of evidence 28 , involving the superior colliculus, pulvinar, and amygdala. The amygdala has been implicated in orienting toward faces in primates, and amygdala lesions impair this tendency for both real and illusory faces 3 . Along with the timescale of the early confusion we observe between real and illusory face processing, this is suggestive of a possible role for the amygdala in falsely detecting faces in everyday objects.…”

Section: Discussionmentioning

confidence: 99%

Rapid and dynamic processing of face pareidolia in the human brain

et al. 2020

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The human brain is specialized for face processing, yet we sometimes perceive illusory faces in objects. It is unknown whether these natural errors of face detection originate from a rapid process based on visual features or from a slower, cognitive re-interpretation. Here we use a multifaceted approach to understand both the spatial distribution and temporal dynamics of illusory face representation in the brain by combining functional magnetic resonance imaging and magnetoencephalography neuroimaging data with model-based analysis. We find that the representation of illusory faces is confined to occipital-temporal face-selective visual cortex. The temporal dynamics reveal a striking evolution in how illusory faces are represented relative to human faces and matched objects. Illusory faces are initially represented more similarly to real faces than matched objects are, but within ~250 ms, the representation transforms, and they become equivalent to ordinary objects. This is consistent with the initial recruitment of a broadly-tuned face detection mechanism which privileges sensitivity over selectivity.

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“…The eyes of others became a more prominent signal along evolution due to anatomical changes in facial morphology that have forced a shift in salience from the shape of the face to the eyes 2 . The importance of the amygdala in processing of eye-gaze was shown in humans and in macaques 13,18,23,[47][48][49][50][51] . Here, we recorded neural activity in the amygdala and the ACC during live interactions in a modified version of the human intruder test (HIT) that includes also a conditioning paradigm.…”

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confidence: 99%

Shared neural codes for eye-gaze and valence

Pryluk

Shohat

Morozov

et al. 2019

Preprint

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The eye-gaze of others is a prominent social cue in primates and crucial for communication [1][2][3][4][5][6][7] , and atypical processing occurs in several conditions as autism-spectrum-disorder (ASD) 1,[9][10][11][12][13][14] . The neural mechanisms that underlie eye-gaze remain vague, and it is still debated if these computations developed in dedicated neural circuits or shared with non-social elements. In many species, eye-gaze signals a threat and elicits anxiety, yet can also serve as a predictor for the outcome of the encounter: negative or positive 2,4,8 . Here, we hypothesized and find that neural codes overlap between eye-gaze and valence. Monkeys participated in a modified version of the human-intruder-test 8,15 that includes direct and averted eye-gaze and interleaved with blocks of aversive and appetitive conditioning 16,17 . We find that singleneurons in the amygdala encode gaze 18 , whereas neurons in the anterior-cingulate-cortex encode the social context 19,20 but not gaze. We identify a shared amygdala circuitry where neural responses to averted and direct gaze parallel the responses to appetitive and aversive value, correspondingly. Importantly, we distinguish two shared coding mechanisms: a shared-intensity scheme that is used for gaze and the unconditioned-stimulus, and a shared-activity scheme that is used for gaze and the conditioned-stimulus. The shared-intensity points to overlap in circuitry, whereas the shared-activity requires also correlated activity. Our results demonstrate that eye-gaze is coded as a signal of valence, yet also as the expected value of the interaction. The findings may suggest new insights into the mechanisms that underlie the malfunction of eye-gaze in ASD and the comorbidity with impaired social skills and anxiety. Haran and Fanny Attar for MRI procedures. This work was supported by ISF #2352/19 and ERC-2016-CoG #724910 grants to R. Paz. Main textRecognizing and learning about potentially harmful or beneficial stimuli is crucial for survival of all organisms. In humans and primates in general, facial expressions, and in particular eye gaze of others, are a prominent and instructive signal 2-7 . Averted or directed eye-gaze is a social signal that can indicate submissive vs. aggressive interactions, correspondingly. In agreement with this, eye-gaze was shown to elicit anxiety in primates 4,8 , and evoke responses in the amygdala 18,21-28 -a brain region that serves as a hub for emotional responses in general and anxiety in particular 25,29,30 . Moreover, gaze processing is disrupted in several neurodevelopmental and social disorders 1,[9][10][11][12] , and mainly in autism-spectrumdisorder (ASD) where abnormal activity of the amygdala is linked to gaze avoidance 13,14 . However, eyegaze is not only a valence-signal by itself, but can also serve as a predictor for future outcomes: aversive if an intruder makes direct eye-contact, or potentially rewarding if the intruder avoids eye-contact. This is in line with the amygdala not only playing a role in signaling outcom...

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Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys

Cited by 69 publications

References 52 publications

Amygdala controls saccade and gaze physically, motivationally, and socially

Amygdala controls saccade and gaze physically, motivationally, and socially

Rapid and dynamic processing of face pareidolia in the human brain

Shared neural codes for eye-gaze and valence

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