Impaired fixation to eyes following amygdala damage arises from abnormal bottom-up attention

SM is a patient with complete bilateral amygdala lesions who fails to fixate the eyes in faces and is consequently impaired in recognizing fear (Adolphs et al., 2005). Here we first replicated earlier findings in SM of reduced gaze to the eyes when seen in whole faces. Examination of the time course of fixations revealed that SM's reduced eye contact is particular pronounced in the first fixation to the face, and less abnormal in subsequent fixations. In a second set of experiments, we used a gaze-contingent presentation of faces with real time eye tracking, wherein only a small region of the face is made visible at the center of gaze. In essence, viewers explore the face by moving a small searchlight over the face with their gaze. Under such viewing conditions, SM's fixations to eye region of faces became entirely normalized. We suggest that this effect arises from the absence of bottom-up effects due to the facial features, allowing gaze location to be driven entirely by top-down control. Together with SM's failure to fixate the eyes in whole faces primarily at the very first saccade, the findings suggest that the saliency of the eyes normally attract our gaze in an amygdala-dependent manner. Impaired eye gaze is also a prominent feature of several psychiatric illnesses in which the amygdala has been hypothesized to be dysfunctional, and our findings and experimental manipulation may hold promise for interventions in such populations, including autism and fragile X syndrome

Human Amygdala Sensitivity to the Pupil Size of Others

Stimulation of the amygdala produces pupil dilation in animal and human subjects. The present study examined whether the amygdala is sensitive to variations in the pupil size of others. Male subjects underwent event-related functional magnetic resonance imaging while passively viewing unfamiliar female faces whose pupils were either unaltered (natural variations in large and small pupils) or altered to be larger or smaller than their original size. Results revealed that the right amygdala and left amygdala/substantia innominata were sensitive to the pupil size of others, exhibiting increased activity for faces with relatively large pupils. Upon debrief, no subject reported being aware that the pupils had been manipulated. These results suggest a function for the amygdala in the detection of changes in pupil size, an index of arousal and/or interest on the part of a conspecific, even in the absence of explicit knowledge

Fear, faces, and the human amygdala

The amygdala's historical role in processing stimuli related to threat and fear is being modified to suggest a role that is broader and more abstract. Amygdala lesions impair the ability to seek out and make use of the eye region of faces, resulting in impaired fear perception. Other studies in rats and humans revive earlier proposals that the amygdala is important not only for fear perception as such, but also for detecting saliency and biological relevance. Debates about some features of this processing now suggest that while the amygdala can process fearful facial expressions in the absence of conscious perception, and while there is some degree of preattentive processing, this depends on the context and is not necessarily more rapid than cortical processing routes. A large current research effort extends the amygdala's putative role to a number of psychiatric illnesses

Amygdala Engagement in Response to Subthreshold Presentations of Anxious Face Stimuli in Adults with Autism Spectrum Disorders: Preliminary Insights

Current theoretical models of autism spectrum disorders (ASD) have proposed that impairments in the processing of social/emotional information may be linked to amygdala dysfunction. However, the extent to which amygdala functions are compromised in ASD has become a topic of debate in recent years. In a jittered functional magnetic resonance imaging study, sub-threshold presentations of anxious faces permitted an examination of amygdala recruitment in 12 high functioning adult males with ASD and 12 matched controls. We found heightened neural activation of the amygdala in both high functioning adults with ASD and matched controls. Neither the intensity nor the time-course of amygdala activation differed between the groups. However, the adults with ASD showed significantly lower levels of fusiform activation during the trials compared to controls. Our findings suggest that in ASD, the transmission of socially salient information along sub-cortical pathways is intact: and yet the signaling of this information to structures downstream may be impoverished, and the pathways that facilitate subsequent processing deficient

Facilitated Orienting Underlies Fearful Face Enhanced Gaze Cueing of Spatial Location

Faces provide a platform for non-verbal communication through emotional expression and eye gaze. Fearful facial expressions are salient indicators of potential threat within the environment, which automatically capture observers’ attention. However, the degree to which fearful facial expressions facilitate attention to others’ gaze is unresolved. Given that fearful gaze indicates the location of potential threat, it was hypothesized that fearful gaze facilitates location processing. To test this hypothesis, a gaze cueing study with fearful and neutral faces assessing target localization was conducted. The task consisted of leftward, rightward, and forward/straight gaze trials. The inclusion of forward gaze trials allowed for the isolation of orienting and disengagement components of gaze-directed attention. The results suggest that both neutral and fearful gaze modulates attention through orienting and disengagement components. Fearful gaze, however, resulted in quicker orienting than neutral gaze. Thus, fearful faces enhance gaze cueing of spatial location through facilitated orienting

A Cross-Linguistic Preference For Torso Stability In The Lexicon: Evidence From 24 Sign Languages

When the arms move in certain ways, they can cause the torso to twist or rock. Such extraneous torso movement is undesirable, especially during sign language communication, when torso position may carry linguistic significance, so we expend effort to resist it when it is not intended. This so-called “reactive effort” has only recently been identified by Sanders and Napoli (2016), but their preliminary work on three genetically unrelated languages suggests that the effects of reactive effort can be observed cross-linguistically by examination of sign language lexicons. In particular, the frequency of different kinds of manual movements in the lexicon correlates with the amount of reactive effort needed to resist movement of the torso. Following this line of research, we present evidence from 24 sign languages confirming that there is a cross-linguistic preference for minimizing the reactive effort needed to keep the torso stable

Single-Unit Responses Selective for Whole Faces in the Human Amygdala

The human amygdala is critical for social cognition from faces, as borne out by impairments in recognizing facial emotion following amygdala lesions and differential activation of the amygdala by faces. Single-unit recordings in the primate amygdala have documented responses selective for faces, their identity, or emotional expression, yet how the amygdala represents face information remains unknown. Does it encode specific features of faces that are particularly critical for recognizing emotions (such as the eyes), or does it encode the whole face, a level of representation that might be the proximal substrate for subsequent social cognition? We investigated this question by recording from over 200 single neurons in the amygdalae of seven neurosurgical patients with implanted depth electrodes. We found that approximately half of all neurons responded to faces or parts of faces. Approximately 20% of all neurons responded selectively only to the whole face. Although responding most to whole faces, these neurons paradoxically responded more when only a small part of the face was shown compared to when almost the entire face was shown. We suggest that the human amygdala plays a predominant role in representing global information about faces, possibly achieved through inhibition between individual facial features

The Look of Fear from the Eyes Varies with the Dynamic Sequence of Facial Actions

Most research on the ability to interpret expressions from the eyes has utilized static information. This research investigates whether the dynamic sequence of facial actions in the eye region influences the judgments of perceivers. Dynamic fear expressions involving the eye region and eyebrows were created which systematically differed in the sequential occurrence of facial actions. Participants rated the intensity of sequential fear expressions, either in addition to a simultaneous, full-blown expression (Experiment 1) or in combination with different levels of eye gaze (Experiment 2). The results showed that the degree of attributed emotion and the appraisal ratings differed as a function of the sequence of facial expressions of fear, with direct gaze resulting in stronger subjective responses. The findings challenge current notions surrounding the study of static facial displays from the eyes and suggest that emotion perception is a dynamic process shaped by the time course of the facial actions of an expression. Possible implications for the field of affective computing and clinical research are discussed