Neurons in the Monkey Amygdala Detect Eye Contact during Naturalistic Social Interactions

In the paper

“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”

What the sources say

• Not checked yetcites [e.g., 21-24]

In the paper

“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.”

In the paper

“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).”

In the paper

“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).”

In the paper

“Direct gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status [3-6].”

What the sources say

• Not checked yetcites [3] Maestripieri, 1997, Affiliative and submissive communication in rhesus macaques, Primates source
• Not checked yetcites [4] Redican, 1975, Facial expressions in nonhuman primates
• Not checked yetcites [5] Gomez, 1996, Ostensive behavior in great apes: the role of eye contact
• Not checked yetcites [6] Baron-Cohen, 1992, Reading the eyes: evidence for the role of perception in the development of a theory of mind, Mind Lang. source

In the paper

“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].”

What the sources say

• Not checked yetcites [2] Emery, 2000, The eyes have it: the neuroethology, function and evolution of social gaze, Neurosci. Biobehav. Rev. source

In the paper

“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].”

What the sources say

• Not checked yetcites [12] Capitanio, 2002, Sociability and responses to video playbacks in adult male rhesus monkeys (Macaca mulatta), Primates source
• Not checked yetcites [13] Ghazanfar, 2006, Eye movements of monkey observers viewing vocalizing conspecifics, Cognition source
• Not checked yetcites [14] Paukner, 2006, Video-induced yawning in stumptail macaques (Macaca arctoides), Biol. Lett. source
• Not checked yetcites [15] Machado, 2011, Social and nonsocial content differentially modulates visual attention and autonomic arousal in Rhesus macaques, PLoS ONE source
• Not checked yetcites [16] Feneran, 2013, Monkey see, monkey do: contagious itch in nonhuman primates, Acta Derm. Venereol. source
• Not checked yetcites [17] Mosher, 2011, Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys, Behav. Neurosci. source
• Not checked yetcites [18] Chang, 2013, Neuronal reference frames for social decisions in primate frontal cortex, Nat. Neurosci. source
• Not checked yetcites [19] Livneh, 2012, Self-monitoring of social facial expressions in the primate amygdala and cingulate cortex, Proc. Natl. Acad. Sci. USA source
• Not checked yetcites [20] Caruana, 2011, Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey, Curr. Biol. source

In the paper

“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.”

In the paper

“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].”

What the sources say

• Not checked yetcites [21] Sanghera, 1979, Visual responses of neurons in the dorsolateral amygdala of the alert monkey, Exp. Neurol. source
• Not checked yetcites [22] Leonard, 1985, Neurons in the amygdala of the monkey with responses selective for faces, Behav. Brain Res. source
• Not checked yetcites [23] Nakamura, 1992, Activity of single neurons in the monkey amygdala during performance of a visual discrimination task, J. Neurophysiol. source
• Not checked yetcites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source
• Not checked yetcites [25] Mosher, 2010, Response characteristics of basolateral and centromedial neurons in the primate amygdala, J. Neurosci. source

In the paper

“These identity-selective cells further differentiate between the facial expressions of that particular individual (see Figure 5 in [24]).”

What the sources say

• Not checked yetcites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source

In the paper

“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.”

What the sources say

• Not checked yetcites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source

In the paper

“Face-selective cells show additional selectivity for individuals.”

What the sources say

• Not checked yetcites [24] Gothard, 2007, Neural responses to facial expression and face identity in the monkey amygdala, J. Neurophysiol. source

In the paper

“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.”

In the paper

“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].”

What the sources say

• Not checked yetcites [3] Maestripieri, 1997, Affiliative and submissive communication in rhesus macaques, Primates source
• Not checked yetcites [4] Redican, 1975, Facial expressions in nonhuman primates
• Not checked yetcites [37] Chance, 1967, Attention structure as the basis of primate rank orders, Man (Lond)

In the paper

“Neurons in TE, however, exhibit heightened sensitivity for details that fall within the fovea [32-34].”

What the sources say

• Not checked yetcites [32] Moran, 1985, Selective attention gates visual processing in the extrastriate cortex, Science source
• Not checked yetcites [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
• Not checked yetcites [34] Rolls, 2003, The receptive fields of inferior temporal cortex neurons in natural scenes, J. Neurosci. source

In the paper

“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.”

In the paper

“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.”

What the sources say

• Not checked yetcites [35] Peck, 2013, The primate amygdala combines information about space and value, Nat. Neurosci. source

In the paper

“In humans, the majority of psychiatric and neurodevelopmental disorders show disruption in the use of eyes and eye contact during social interactions [38-42].”

What the sources say

• Not checked yetcites [38] Jones, 2013, Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism, Nature source
• Not checked yetcites [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
• Not checked yetcites [40] Hirstein, 2001, Autonomic responses of autistic children to people and objects, Proc. Biol. Sci. source
• Not checked yetcites [41] Tso, 2012, Eye-contact perception in schizophrenia: relationship with symptoms and socioemotional functioning, J. Abnorm. Psychol. source
• Not checked yetcites [42] Schneier, 2011, Fear and avoidance of eye contact in social anxiety disorder, Compr. Psychiatry source

In the paper

“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].”

What the sources say

• Not checked yetcites [26] Desimone, 1989, Neural mechanisms of visual processing in monkeys
• Not checked yetcites [27] Herzog, 1976, Temporal neocortical afferent connections to the amygdala in the rhesus monkey, Brain Res. source
• Not checked yetcites [28] Amaral, 1984, Amygdalo-cortical projections in the monkey (Macaca fascicularis), J. Comp. Neurol. source
• Not checked yetcites [29] Gross, 1969, Visual receptive fields of neurons in inferotemporal cortex of the monkey, Science source
• Not checked yetcites [30] Boussaoud, 1991, Visual topography of area TEO in the macaque, J. Comp. Neurol. source
• Not checked yetcites [31] Freiwald, 2010, Functional compartmentalization and viewpoint generalization within the macaque face-processing system, Science source

In the paper

“For example, patients on the autism spectrum typically fail to solicit and reciprocate eye contact [40,43-45].”

What the sources say

• Not checked yetcites [40] Hirstein, 2001, Autonomic responses of autistic children to people and objects, Proc. Biol. Sci. source
• Not checked yetcites [43] Kliemann, 2012, The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders, J. Neurosci. source
• Not checked yetcites [44] Tanaka, 2013, The “Eye Avoidance” Hypothesis of Autism Face Processing, J. Autism Dev. Disord. source
• Not checked yetcites [45] Rutishauser, 2013, Single-neuron correlates of atypical face processing in autism, Neuron source