Neurons in the Monkey Amygdala Detect Eye Contact during Naturalistic Social Interactions
Open accessAbstract
Summary Primates explore the visual world through eye-movement sequences. Saccades bring details of interest into the fovea while fixations stabilize the image [1]. During natural vision, social primates direct their gaze at the eyes of others to communicate their own emotions and intentions and to gather information about the mental states of others [2]. Direct gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status [3-6]. Despite the great importance of making and breaking eye contact in the behavioral repertoire of primates, little is known about the neural substrates that support these behaviors. Here we show that the monkey amygdala contains neurons that respond selectively to fixations at the eyes of others and to eye contact. These “eye cells” share several features with the canonical, visually responsive neurons in the monkey amygdala, however, they respond to the eyes only when they fall within the fovea of the viewer, either as a result of a deliberate saccade, or as eyes move into the fovea of the viewer during a fixation intended to explore a different feature. The presence of eyes in peripheral vision fails to activate the eye cells. These findings link the primate amygdala to eye-movements involved in the exploration and selection of details in visual scenes that contain socially and emotionally salient features.
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Written from the paper’s full text.
TL;DR
The monkey amygdala contains neurons that respond selectively when another monkey’s eyes fall in the fovea, including a subpopulation that distinguishes direct eye contact from averted gaze. These “eye cells” show nested selectivity with canonical visually responsive amygdala neurons and may support gaze-mediated social behavior.
Key findings
Of 318 well-isolated neurons, 38 (12%) significantly changed firing rate when subjects fixated the eyes of movie monkeys (Q: 8/104, 7.7%; Z: 27/171, 15.8%; G: 3/42, 7.1%); these cells did not respond, or responded less, to fixations on the mouth, and 14 additional cells responded to all fixations independent of target.
- A subpopulation of 10 eye-fixation cells fired significantly more during eye contact than during fixations on averted eyes; one example increased up to 76 Hz during eye contact versus a mean 10 Hz during averted-eye fixations, with a 5 Hz baseline. Two cells instead responded more to averted gaze (cell 1: 15.2 Hz vs. 7.7 Hz; cell 2: 12.0 Hz vs. 9.7 Hz).
- Eye cells responded only when eyes were in the fovea, not in peripheral vision; saccades were not necessary. Five eye-fixation cells responded similarly after saccades to the eyes and passive appearance of eyes at fixation (latency 121±27 ms vs. 133±74 ms; t3=−0.574, P=0.697).
- Eye cells appear to be a specialized class of visually responsive amygdala neurons: 248/318 (78%) responded to video onset/offset, all 52 fixation cells responded to visual stimuli, and 52/248 (21%) of visually responsive cells also responded to eye fixations.
Methods
Recorded neuronal activity from the amygdalae of three monkeys (Q, Z, G) while they viewed videos of natural behaviors by unfamiliar conspecifics; two subjects also viewed static frames extracted from each video.
- Identified fixations on facial features and periods of eye contact by combining the viewer’s scanpath with an ethogram marking the movie monkey’s gaze direction.
- Main analyses included Wilcoxon rank-sum tests for fixation-related firing changes, bootstrap shuffling of the movie-monkey ethogram for eye-contact selectivity, t-tests/chi-square comparisons, and histology/recording-site reconstruction; additional paradigms tested static images and cue-triggered face presentation with eyes at the fovea or >4° from center.
Limitations
Stated: the design precluded analyses of higher-order levels such as eye contact during appeasing or affiliative interactions, or eye contact with a friend versus a foe; the authors also note that a more complete answer on eye-contact cells is expected from a larger population.
- Evident: key subpopulations were small—10 eye-contact cells, only 2 eye-contact cells tested with static images, 5 eye-fixation cells in the passive-viewing paradigm, and 3 nonselective-fixation cells—limiting generalizability.
- Evident: the study is recording-based and does not causally manipulate eye cells; the authors state that future studies blocking or enhancing eye-cell activity are needed.
Model-written summary. Check it against the paper before relying on it.
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Cites
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Claims the paper makes
0 of 55 cited sources checked · 0 supported · 0 flagged
- Findingown data
Monkeys spent significantly less time fixating the mouth than the eyes.
“They spent significantly less time fixating the mouth: Chi-squared test comparing the percent of time that the eyes or mouth were fixated, P <0.00001”
Quote in the paperNot a substantial claim - Findingown data
Eye cells respond to the eyes only when they fall within the fovea of the viewer, either as a result of a deliberate saccade or as eyes move into the fovea during a fixation intended to explore a different feature.
“they respond to the eyes only when they fall within the fovea of the viewer, either as a result of a deliberate saccade, or as eyes move into the fovea of the viewer during a fixation intended to explore a different feature.”
Quote in the paperSubstantial claim - Findingown data
The presence of eyes in peripheral vision fails to activate the eye cells.
“The presence of eyes in peripheral vision fails to activate the eye cells.”
Quote in the paperSubstantial claim - Findingown data
The monkey amygdala contains neurons that respond selectively to fixations at the eyes of others and to eye contact.
“Here we show that the monkey amygdala contains neurons that respond selectively to fixations at the eyes of others and to eye contact.”
Quote in the paperSubstantial claim - Findingnone given
Eye cells share several features with the canonical, visually responsive neurons in the monkey amygdala.
“These “eye cells” share several features with the canonical, visually responsive neurons in the monkey amygdala”
Quote in the paperNot a substantial claim
- Findingown data
Monkeys Q, Z, and G spent 39.1%, 26.8%, and 17.2% of time fixating the eyes of movie monkeys, even though the eyes occupied only 2.6% of the video frames.
“even though the eyes occupied only 2.6% of the video frames, monkeys Q, Z, and G spent 39.1%, 26.8%, and 17.2% fixating them.”
Quote in the paperNot a substantial claim0 of 5 sources checked- cites [7] Keating, 1982, Visual scan patterns of rhesus monkeys viewing faces, Perception source
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- cites [8] Nahm, 1997, How do monkeys look at faces?, J. Cogn. Neurosci. source
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- cites [9] Parr, 2000, Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta), J. Comp. Psychol. source
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- cites [10] Gibboni, 2009, Individual differences in Scanpaths correspond with serotonin transporter genotype and behavioral phenotype in rhesus monkeys (Macaca mulatta), Front. Behav. Neurosci. source
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- cites [11] Payne, 2013, Crossmodal integration of conspecific vocalizations in rhesus macaques, PLoS ONE source
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- Findingown data
Eye-contact selective cells increased their firing rate when the movie monkey changed its direction of gaze from averted to direct while the viewer fixated the eyes.
“Indeed, the eye-contact selective cells increased their firing rate when the movie monkey changed its direction of gaze from averted to direct while the viewer fixated the eyes (e.g., Figure 3B and 3D at 3.3 s and 3.5 s, respectively).”
Quote in the paperSubstantial claim - Findingown data
The average activity of all 318 recorded cells indicates that the population responded more strongly during fixations on the eyes than during fixations on other features.
“The average activity of all 318 recorded cells indicates that the population responded more strongly during fixations on the eyes than during fixations on other features (Figure S1 B, bottom panel).”
Quote in the paperSubstantial claim - Findingown data
One neuron increased its firing rate up to 76 Hz during eye-contact compared to a mean rate of 10 Hz during fixations on averted eyes, with a baseline firing rate of 5 Hz.
“The high sensitivity to eye-contact is illustrated by an increase of up to a 76 Hz firing rate during eye-contact compared to a mean rate of 10 Hz during fixations on averted eyes for a neuron with a baseline firing rate of 5 Hz (Figure 3, Movie S3).”
Quote in the paperNot a substantial claim - Findingown data
Three nonselective-fixation cells tested responded similarly to the appearance of any feature at the center of gaze.
“By comparison, three nonselective-fixation cells were tested in this paradigm and these responded similarly to the appearance of any feature at the center of the gaze (Figure S3 E) (t-test comparing mean firing rate, t2=1.512, P=0.135).”
Quote in the paperSubstantial claim - Findingown data
Two eye-contact cells tested with static images responded during fixations on eyes with direct gaze (the equivalent of eye contact) with elevated firing rates (mean rate during eye contact and during fixations on averted eyes: cell 1: 19.7 Hz, 28.3 Hz; cell 2: 7.1 Hz, 9.7 Hz).
“Two eye-contact cells were also tested with static images. Both cells responded during fixations on eyes with direct gaze (the equivalent of eye contact) with elevated firing rates (mean rate during eye contact and during fixations on averted eyes: cell 1: 19.7 Hz, 28.3 Hz; cell 2: 7.1 Hz, 9.7 Hz).”
Quote in the paperSubstantial claim - Findingown data
The temporal patterns of spike trains (phasic vs. tonic responses) were similar during eye-fixations on dynamic and static stimuli.
“The temporal patterns of the spike trains, i.e., phasic vs. tonic responses, were similar during eye-fixations on dynamic and static stimuli.”
Quote in the paperSubstantial claim - Findingown data
Videos captured the viewer's attention for longer periods of time than static images, as measured by time spent fixating the eyes (monkeys Z and G).
“Indeed, videos captured the viewer’s attention for longer periods of time (paired t-test comparing time spent fixating the eyes of videos and the eyes of static images: Z, t2234=14.08, P<0.00001; G, t2791=7.99, P<0.00001).”
Quote in the paperNot a substantial claim - Findingown data
Fourteen cells responded to all fixations independent of the target.
“We found, however, 14 cells that responded to all fixations independent of the target (Figure 2E).”
Quote in the paperNot a substantial claim - Findingown data
Two eye-fixation cells responded with significantly greater firing rates during fixations on eyes with averted gaze than during eye contact (cell 1: 15.2 Hz vs 7.7 Hz; cell 2: 12.0 Hz vs 9.7 Hz).
“By contrast, two cells responded with significantly greater firing rates during fixations on eyes with averted gaze (mean rate during eye contact and during fixations on averted eyes: cell 1: 15.2 Hz, 7.7 Hz; cell 2: 12.0 Hz, 9.7 Hz).”
Quote in the paperNot a substantial claim - Findingown data
Nonspecific fixation cells and eye cells share the properties of visually-responsive neurons in the amygdala.
“The nonspecific fixation cells and the eye cells share these properties with the rest of visually-responsive neurons in the amygdala.”
Quote in the paperSubstantial claim - Findingown data
Eye-fixation cells did not respond, or responded with a reduced firing rate, when subjects fixated other facial features, e.g., the mouth.
“These “eye-fixation cells” did not respond (or responded with a reduced firing rate), when subjects fixated other facial features, e.g., the mouth (Wilcoxon rank-sum test, P <0.05, Supplementary Data Analysis).”
Quote in the paperSubstantial claim - Findingown data
A group of 10 eye-fixation cells responded with significantly higher firing rates during eye-contact than during fixations at eyes with averted gaze.
“A group of 10 eye-fixation cells responded with significantly higher firing rates during eye-contact than during fixations at eyes with averted gaze (Figure 3) (two-tail bootstrap by shuffling movie-monkey ethogram, P <0.05, Supplementary Experimental Procedures).”
Quote in the paperSubstantial claim - Findingown data
The response of fixation-cells to the onset of visual stimuli is independent of the monkey's subsequent eye-movements.
“It is critical to emphasize that the response of fixation-cells to the onset of visual stimuli is independent of the monkey’s subsequent eye-movements.”
Quote in the paperSubstantial claim - Findingown data
Eye cells responded differentially to the eyes compared to the mouth for both the active and passive looking conditions.
“These cells responded differentially to the eyes compared to the mouth for both the active and passive looking conditions (mean difference in firing rate to static images with central presentation on eyes compared to mouth: 15.5+6.2 Hz, 46.2+18.5% ; paired t-test, t4=5.5939, P=0.005).”
Quote in the paperSubstantial claim - Findingown data
Fixating the eyes of dynamic and static images induced similar changes in firing rate in eye-fixation cells.
“Fixating the eyes of dynamic and static images induced similar changes in firing rate (Figure 4) (mean difference in rate 0.63±3.57 Hz , equivalent to a 7±25% change; t13=-0.6598, P=0.529).”
Quote in the paperSubstantial claim - Findingown data
The pattern of response (tonic vs. phasic and inhibitory or excitatory) of fixation cells was preserved for images, fixations, and the content of fixations.
“Moreover, the pattern of their response (tonic vs. phasic and inhibitory or excitatory) was preserved for images, fixations, and the content of fixations (Figure S4 A-B and S4 C-D).”
Quote in the paperSubstantial claim - Findingown data
Of 318 recorded neurons, 248 (78%) responded to the onset/offset of the presence of videos depicting conspecifics.
“Re-examining our 318 recorded neurons in this light, 248 (78%) responded to the onset/offset of the presence of videos depicting conspecifics.”
Quote in the paperSubstantial claim - Findingown data
Nonselective-fixation cells were the only other type of fixation-related neuron identified.
“These “nonselective-fixation cells” were the only other type of fixation-related neuron identified.”
Quote in the paperNot a substantial claim - Findingown data
The same analysis applied to fixations on other facial features failed to identify cells selective for any other targets.
“The same analysis applied to fixations on other facial features (e.g., the mouth) failed to identify cells that were selective for any other targets.”
Quote in the paperSubstantial claim - Findingown data
Eye fixation cells were not topographically clustered (4/45, 9% in centromedial and 34/273, 12% in basolateral nuclei).
“The eye fixation cells were not topographically clustered (Figure S2, histology and recording site reconstruction) (4/45, 9% in the centromedial and 34/273, 12%, in the basolateral nuclei; Yates chi-square: χ2df=1=0.189, P=0.664).”
Quote in the paperNot a substantial claim - Findingown data
Of 318 well-isolated neurons, 38 neurons (12%) significantly changed their firing rate when the subjects fixated the eyes of the movie monkeys.
“Of 318 well-isolated neurons, 38 neurons (12%) significantly changed their firing rate when the subjects fixated the eyes of the movie monkeys (Wilcoxon rank-sum test, P<0.05; Q: 8/104 cells, 7.7%; Z: 27/171 cells, 15.8%; G: 3/42 cells, 7.1%)”
Quote in the paperSubstantial claim - Findingown data
In all instances, the neural response for stimulus onset preceded the neural response elicited by the first fixation.
“In all instances the neural response for stimulus onset preceded the neural response elicited by the first fixation that the monkeys made (latency of neural response following onset of video stimuli: 147+56 ms; latency of first eye-movement on the visual stimuli: 251+91 ms, ranksum test: z=6.451, P<0.0001).”
Quote in the paperSubstantial claim - Findingown data
The neural response evoked by the visual stimulus is more strongly time-locked to the appearance of the stimulus than to the first fixation on that stimulus.
“Indeed, the neural response evoked by the visual stimulus is more strongly time-locked to the appearance of the stimulus than the first fixation on that stimulus (maximum response rate when aligned to onset of visual stimulus vs. first fixation: 50.3±43.59 Hz vs. 34.8±25.9, signed rank test, z=5.655, P<0.0001).”
Quote in the paperSubstantial claim - Interpretationreasoning
These findings link the primate amygdala to eye-movements involved in the exploration and selection of details in visual scenes that contain socially and emotionally salient features.
“These findings link the primate amygdala to eye-movements involved in the exploration and selection of details in visual scenes that contain socially and emotionally salient features.”
Quote in the paperSubstantial claim - Premisecitation
Selectivity for the content of images in amygdala neurons is expressed by changes in the polarity of the response, the magnitude of the response, and the temporal pattern of the response.
“We have previously shown that selectivity for the content of the images is expressed by changes in (1) the polarity of the response, i.e., inhibitory or excitatory, (2) the magnitude of the response, and (3) the temporal pattern of the response (e.g., bursting, phasic, or tonic changes in firing rate) (see Figure 2, in [25]).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [25] Mosher, 2010, Response characteristics of basolateral and centromedial neurons in the primate amygdala, J. Neurosci. source
Not checked in the free run.
- Interpretationown data
These initial findings indicate that eye-contact cells differentiate direct and averted gaze independent of the dynamic/static properties of the stimulus.
“Although a more complete answer is expected to emerge from a larger population of eye contact cells, these initial findings indicate that these cells differentiate direct and averted gaze independent of the dynamic/static properties of the stimulus.”
Quote in the paperSubstantial claim - Premisecitation
Videos engaged the viewer monkeys in socially-meaningful looking behaviors rarely observed in responses to static images.
“The videos engaged the viewer monkeys in socially-meaningful looking behaviors rarely observed in responses to static images [17].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17] Mosher, 2011, Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys, Behav. Neurosci. source
Not checked in the free run.
- Premisecitation
Eye contact, its duration, and the way it is achieved or avoided are meaningful communicative signals.
“Eye contact, its duration, and the way it is achieved or avoided are meaningful communicative signals.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [3] Maestripieri, 1997, Affiliative and submissive communication in rhesus macaques, Primates source
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- cites [4] Redican, 1975, Facial expressions in nonhuman primates
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- cites [37] Chance, 1967, Attention structure as the basis of primate rank orders, Man (Lond)
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- May combine two claims. 12
- Classified as probably not a substantial claim. 11
May combine two claims.
Findingown dataThe response latency of eye fixation cells varied between 80-140 ms with a mean of 118±29 ms, shorter than the response latency of canonical visually-driven cells in the amygdala (mean 157±58 ms).
“The response latency of the eye fixation cells varied between 80-140 ms with a mean latency of 118±29 ms, which is shorter than the response latency of canonical visually-driven cells in the amygdala (mean response latency to the presentation of visual stimuli: 157±58 ms, paired t-test t56=3.3299, P=0.0015; previously reported latencies of visually-responsive neurons in the amygdala exceed 100 ms”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [e.g., 21-24]
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May combine two claims.
Findingown dataAll five eye-fixation cells tested responded similarly after saccades to the eyes and the appearance of eyes at the center of fixation, indicating that saccades are not necessary for eye-cell activity.
“All five eye-fixation cells responded similarly after saccades to the eyes and the appearance of eyes at the center of fixation (Figure S3 B-D) indicating that saccades are not a sine qua non requirement for the activity of eye cells.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThe response patterns of eye-fixation cells during fixation at the eyes were tonic excitation spanning the entire fixation, phasic excitation with an average duration of 120±42 ms, and phasic inhibition.
“The response patterns registered during fixation at the eyes were: (1) tonic excitation spanning the entire duration of fixations at the eyes (Figure 2B), (2) phasic excitation with an average duration of 120±42 ms (Figure 2C), and (3) phasic inhibition (Figure 2D).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataAll 52 identified fixation cells (38 eye fixation cells and 14 non-selective fixation cells) responded to the appearance of visual stimuli on the monitor and the presence of eyes in the fovea; 52/248 (21%) of visually responsive cells also responded to fixations on the eyes.
“All 52 identified fixation cells (38 eye fixation cells and 14 non-selective fixation cells), responded to the appearance of visual stimuli on the monitor and the presence of eyes in the fovea (i.e., 52/248, 21%, of the visually responsive cells also responded to fixations on the eyes; Figure S4).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationDirect gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status.
“Direct gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status [3-6].”
Quote in the paperNot a substantial claim0 of 4 sources checked- cites [3] Maestripieri, 1997, Affiliative and submissive communication in rhesus macaques, Primates source
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- cites [4] Redican, 1975, Facial expressions in nonhuman primates
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- cites [5] Gomez, 1996, Ostensive behavior in great apes: the role of eye contact
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- cites [6] Baron-Cohen, 1992, Reading the eyes: evidence for the role of perception in the development of a theory of mind, Mind Lang. source
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Classified as probably not a substantial claim. May combine two claims.
PremisecitationDuring natural vision, social primates direct their gaze at the eyes of others to communicate their own emotions and intentions and to gather information about the mental states of others.
“During natural vision, social primates direct their gaze at the eyes of others to communicate their own emotions and intentions and to gather information about the mental states of others [2].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [2] Emery, 2000, The eyes have it: the neuroethology, function and evolution of social gaze, Neurosci. Biobehav. Rev. source
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PremisecitationVideos promote interactive looking behaviors, e.g., eye contact, gaze-following, gaze-avoidance, and the reciprocation of facial expressions, as they better approximate natural interactions.
“We have previously shown that videos promote interactive looking behaviors, e.g., eye contact, gaze-following, gaze-avoidance, and the reciprocation of facial expressions [12-17] as they better approximate natural interactions [18-20].”
Quote in the paperSubstantial claim0 of 9 sources checked- cites [12] Capitanio, 2002, Sociability and responses to video playbacks in adult male rhesus monkeys (Macaca mulatta), Primates source
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- cites [13] Ghazanfar, 2006, Eye movements of monkey observers viewing vocalizing conspecifics, Cognition source
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- cites [14] Paukner, 2006, Video-induced yawning in stumptail macaques (Macaca arctoides), Biol. Lett. source
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- cites [15] Machado, 2011, Social and nonsocial content differentially modulates visual attention and autonomic arousal in Rhesus macaques, PLoS ONE source
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- cites [16] Feneran, 2013, Monkey see, monkey do: contagious itch in nonhuman primates, Acta Derm. Venereol. source
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- cites [17] Mosher, 2011, Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys, Behav. Neurosci. source
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- cites [18] Chang, 2013, Neuronal reference frames for social decisions in primate frontal cortex, Nat. Neurosci. source
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- cites [19] Livneh, 2012, Self-monitoring of social facial expressions in the primate amygdala and cingulate cortex, Proc. Natl. Acad. Sci. USA source
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- cites [20] Caruana, 2011, Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey, Curr. Biol. source
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Interpretationown dataEye cells exhibit a pattern of nested selectivity: a primary response signals the presence of videos, a secondary response signals fixations at eyes, and a tertiary response signals eye contact.
“Thus the primary response of these cells signals the presence of videos while the secondary and tertiary response signals fixations at eyes and eye contact, respectively, in a pattern of nested selectivity.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationMany visually-responsive neurons in the monkey amygdala respond to the onset or offset of visual stimuli (phasic image-on/image-off cells) or to the entire time an image is presented (tonic responses).
“Many visually-responsive neurons in the monkey amygdala respond to the onset or offset of visual stimuli (phasic image-on/image-off cells) or to the entire time an image is presented (tonic responses) [21-25].”
Quote in the paperSubstantial claim0 of 5 sources checked- cites [21] Sanghera, 1979, Visual responses of neurons in the dorsolateral amygdala of the alert monkey, Exp. Neurol. source
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- cites [22] Leonard, 1985, Neurons in the amygdala of the monkey with responses selective for faces, Behav. Brain Res. source
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- cites [23] Nakamura, 1992, Activity of single neurons in the monkey amygdala during performance of a visual discrimination task, J. Neurophysiol. source
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- cites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source
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- cites [25] Mosher, 2010, Response characteristics of basolateral and centromedial neurons in the primate amygdala, J. Neurosci. source
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PremisecitationIdentity-selective cells further differentiate between the facial expressions of that particular individual.
“These identity-selective cells further differentiate between the facial expressions of that particular individual (see Figure 5 in [24]).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source
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PremisecitationThe vast majority of neurons in the amygdala are category selective, responding differentially to monkey faces, human faces, and objects.
“Indeed, our 2007 report on the selectivity of amygdala neurons [24] shows that the vast majority of neurons in the amygdala are category selective, responding differentially to monkey faces, human faces, and objects.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source
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PremisecitationFace-selective cells show additional selectivity for individuals.
“Face-selective cells show additional selectivity for individuals.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source
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InterpretationreasoningThe timing of fixations and saccades is inconsistent across trials, and averaging the spike trains across trials eliminated the chance to observe short-lived fixation-related changes of firing rates, explaining why eye cells were missed in past static-image data.
“Because the timing of fixations and saccades is inconsistent across trials, and averaging the spike trains across trials eliminated the chance to observe these short-lived fixation-related changes of firing rates.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationA confident, dominant monkey initiates eye contact by staring at the eyes of others and waiting for the targeted eyes to return direct gaze; submissive individuals might engage briefly in eye contact or may choose to avoid it altogether.
“A confident, dominant monkey initiates eye contact by staring at the eyes of others and waiting for the targeted eyes to return direct gaze; submissive individuals might engage briefly in eye contact or may choose to avoid it altogether [3,4,37].”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [3] Maestripieri, 1997, Affiliative and submissive communication in rhesus macaques, Primates source
Not checked in the free run.
- cites [4] Redican, 1975, Facial expressions in nonhuman primates
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- cites [37] Chance, 1967, Attention structure as the basis of primate rank orders, Man (Lond)
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Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationNeurons in area TE exhibit heightened sensitivity for details that fall within the fovea.
“Neurons in TE, however, exhibit heightened sensitivity for details that fall within the fovea [32-34].”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [32] Moran, 1985, Selective attention gates visual processing in the extrastriate cortex, Science source
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- cites [33] Rolls, 1995, The responses of single neurons in the temporal visual cortical areas of the macaque when more than one stimulus is present in the receptive field, Exp. Brain Res. source
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- cites [34] Rolls, 2003, The receptive fields of inferior temporal cortex neurons in natural scenes, J. Neurosci. source
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InterpretationreasoningAt the population level, neurons that signal eye contact elicit the highest firing rates, similarly to threatening faces that elicited higher firing rates than neutral and appeasing expressions.
“The idea that, in the amygdala, the most socially salient stimuli elicit the highest firing rates holds true: at the population level neurons that signal eye contact elicit the highest firing rates, similarly to threatening faces that elicited higher firing rates than neutral and appeasing expressions.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationNeurons in the amygdala carry spatial information about the location of rewards, albeit the spatial scale might be too coarse for differentiating between foveal and peripheral presence of eyes.
“Recent reports on the spatial-selectivity of neurons recorded from the amygdala [35] suggest neurons therein carry spatial information about the location of rewards, albeit the spatial scale might be too coarse for differentiating between foveal and peripheral presence of eyes.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [35] Peck, 2013, The primate amygdala combines information about space and value, Nat. Neurosci. source
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PremisecitationIn humans, the majority of psychiatric and neurodevelopmental disorders show disruption in the use of eyes and eye contact during social interactions.
“In humans, the majority of psychiatric and neurodevelopmental disorders show disruption in the use of eyes and eye contact during social interactions [38-42].”
Quote in the paperNot a substantial claim0 of 5 sources checked- cites [38] Jones, 2013, Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism, Nature source
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- cites [39] Rice, 2012, Parsing heterogeneity in autism spectrum disorders: visual scanning of dynamic social scenes in school-aged children, J. Am. Acad. Child Adolesc. Psychiatry source
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- cites [40] Hirstein, 2001, Autonomic responses of autistic children to people and objects, Proc. Biol. Sci. source
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- cites [41] Tso, 2012, Eye-contact perception in schizophrenia: relationship with symptoms and socioemotional functioning, J. Abnorm. Psychol. source
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- cites [42] Schneier, 2011, Fear and avoidance of eye contact in social anxiety disorder, Compr. Psychiatry source
Not checked in the free run.
May combine two claims.
InterpretationcitationRetinotopy in the amygdala is unlikely because visual receptive fields in areas that project to the amygdala, e.g., area TE, are large enough to encompass an entire hemifield.
“Retinotopy is unlikely when considering the gradual expansion of visual receptive fields along the ventral visual pathway [26]; indeed the receptive fields in areas that project to the amygdala, e.g. area TE [27,28], are large enough to encompass an entire hemifield [29-31].”
Quote in the paperNot a substantial claim0 of 6 sources checked- cites [26] Desimone, 1989, Neural mechanisms of visual processing in monkeys
Not checked in the free run.
- cites [27] Herzog, 1976, Temporal neocortical afferent connections to the amygdala in the rhesus monkey, Brain Res. source
Not checked in the free run.
- cites [28] Amaral, 1984, Amygdalo-cortical projections in the monkey (Macaca fascicularis), J. Comp. Neurol. source
Not checked in the free run.
- cites [29] Gross, 1969, Visual receptive fields of neurons in inferotemporal cortex of the monkey, Science source
Not checked in the free run.
- cites [30] Boussaoud, 1991, Visual topography of area TEO in the macaque, J. Comp. Neurol. source
Not checked in the free run.
- cites [31] Freiwald, 2010, Functional compartmentalization and viewpoint generalization within the macaque face-processing system, Science source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPatients on the autism spectrum typically fail to solicit and reciprocate eye contact.
“For example, patients on the autism spectrum typically fail to solicit and reciprocate eye contact [40,43-45].”
Quote in the paperNot a substantial claim0 of 4 sources checked- cites [40] Hirstein, 2001, Autonomic responses of autistic children to people and objects, Proc. Biol. Sci. source
Not checked in the free run.
- cites [43] Kliemann, 2012, The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders, J. Neurosci. source
Not checked in the free run.
- cites [44] Tanaka, 2013, The “Eye Avoidance” Hypothesis of Autism Face Processing, J. Autism Dev. Disord. source
Not checked in the free run.
- cites [45] Rutishauser, 2013, Single-neuron correlates of atypical face processing in autism, Neuron source
Not checked in the free run.
The paper relies on this without support.
Little is known about the neural substrates that support making and breaking eye contact in primates.
“Despite the great importance of making and breaking eye contact in the behavioral repertoire of primates, little is known about the neural substrates that support these behaviors.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The amygdala plays a critical role in allocating attention to other people and in integrating social information and social emotions into decision-making.
“This is consistent with studies showing that the amygdala plays a critical role in allocating attention to other people 7 and in integrating social information 42 and social emotions 13 into decision-making.”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [42]
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Consistentz = 6.451reported p < .0001 · recomputed p < .001
“z=6.451, p < .0001”
- Consistentz = 5.655reported p < .0001 · recomputed p < .001
“z=5.655, p < .0001”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rates contradict the claimed preference for averted gaze
MajorThe rates are listed in eye-contact-then-averted order, and both cells have higher rates during eye contact, contrary to the stated preference for averted gaze.
“two cells responded with significantly greater firing rates during fixations on eyes with averted gaze”
“mean rate during eye contact and during fixations on averted eyes: cell 1: 15.2 Hz, 7.7 Hz; cell 2: 12.0 Hz, 9.7 Hz”
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“These hypothetical mechanisms could account for many of the behavioral effects of OT, for example, increased attention to the eyes is a resultofincreased saliencefor eyestimuli whichare represented in the amygdala (Mosher et al., 2014).”
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Primate amygdala neurons evaluate the progress of self-defined economic choice sequences
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Social determinants of eyeblinks in adult male macaques
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Self-citationTemporal continuity shapes visual responses of macaque face patch neurons
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Self-citationAmygdala activity for the modulation of goal-directed behavior in emotional contexts
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Effects of chronic oxytocin on attention to dynamic facial expressions in infant macaques
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Recognition Memory in Marmoset and Macaque Monkeys: A Comparison of Active Vision
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An Emerging Field of Primate Social Neurophysiology: Current Developments
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Face size biases emotion judgment through eye movement
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Volumetric Analysis of Amygdala and Hippocampal Subfields for Infants with Autism
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Mesoscopic-scale functional networks in the primate amygdala
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Self-citationDevelopment of social systems neuroscience using macaques
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Amygdala growth from youth to adulthood in the macaque monkey
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Neurons in primate prefrontal cortex signal valuable social information during natural viewing
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- Authors
- Mosher, C. P., Zimmerman, P. E., & Gothard, K. M.
- Affiliations
- University of Arizona (US)
- Corresponding author
- Gothard, Katalin M.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2014-10
- Volume
- 24
- Issue
- 20
- Pages
- 2459-2464
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4253056
- OpenAlex
- W2111767565
- Semantic Scholar
- 043aba83b5227e481c022e28be373a179d29e6e9
- Cited by
- 154
- References
- 49
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 16 · 2023: 7 · 2022: 5 · 2021: 17 · 2020: 13 · 2019: 30 · 2018: 12 · 2017: 11 · 2016: 17 · 2015: 8 · 2014: 2 · 2013: 1 · 2012: 1
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UA Campus Repository (The University of Arizona) (acceptedVersion)
- Funders
- National Science Foundation
- U.S. Public Health Service (R21086065)
- National Institute of Mental Health (P50MH100023, R21MH086065)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- eye contact, amygdala, saccades, fixation, fovea, social cognition, primate social behavior, naturalistic social interaction, rhesus monkeys, theory of mind, facial expressions, social communication, visual stability
- MeSH terms
- Amygdala, Animals, Haplorhini, Behavior, Animal, Face, Neurons, Social Behavior, Video Recording, Visual Perception
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.
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